C. R. Guglielmino

Globalization and fruitfly invasion and expansion: the medfly paradigm

The phytophagous insects of the Tephritidae family commonly referred to as “true fruit flies” offer different case histories of successful invasions. Mankind has played an important role in altering the distributions of some of the more polyphagous and oligophagous species. However, the question arises why only a few species have become major invaders. The understanding of traits underlying adaptation in different environments is a major topic in invasion biology. Being generalists or specialists, along the K–r gradient of the growth curve, make a difference in term of food resources exploitation and interspecies competition and displacement. The species of the genus Ceratitis are good examples of r-strategists. The genetic and biological data of the most notorious Ceratitis species, the Mediterranean fruit fly Ceratitis capitata (medfly), are reviewed to investigate the traits and behaviours that make the medfly an important invader. It can be learnt from medfly, that invasions in a modern global trade network tend to be due to multiple introductions. This fact allows a maintenance or enhancement of genetic variability in the adventive populations, which in turn increases their potential invasiveness. Our current knowledge of the medfly genome opens the way for future studies on functional genomics.

Polymorphism within and between populations of Ceratitis capitata: comparison between RAPD and multilocus enzyme electrophoresis data.

Random amplified polymorphic DNA (RAPD) analysis and multilocus enzyme electrophoresis (MLEE) were used to assess genetic variability in six wild populations and in five laboratory strains of Ceratitis capitata. The RAPD technique reveals larger amounts of genetic variation than the conventional MLEE, and can improve discrimination within and between populations and strains. In our experimental conditions, RAPD analysis with four different primers produces 174 polymorphic bands out of 176, while MLEE analysis at 26 enzyme loci scores 74 alleles. RAPD fingerprints are peculiar to African flies, while different laboratory strains have similar patterns, independently of their origins. The results obtained by these two methods are significantly correlated, and are in agreement with the general trend of decreasing variability from African populations towards the peripheral and laboratory ones. UPGMA dendrograms derived from MLEE (protein) and RAPD (DNA) data show that a major part of intraspecific variability involves the differentiation of central vs. peripheral populations.

Microsatellite analysis of medfly bioinfestations in California

The Mediterranean fruit fly, Ceratitis capitata, is a destructive agricultural pest with a long history of invasion success. This pest has been affecting different regions of the United States for the past 30 years, but a number of studies of medfly bioinfestations has focused on the situation in California. Although some progress has been made in terms of establishing the origin of infestations, the overall status of this pest in this area remains controversial. Specifically, do flies captured over the years represent independent infestations or the persistence of a resident population? We present an effort to answer this question based on the use of multilocus genotyping. Ten microsatellite loci were used to analyse 109 medflies captured in several infestations within California between 1992 and 1998. Using these same markers, 242 medflies from regions of the world having ‘established’ populations of this pest including Hawaii, Guatemala, El Salvador, Ecuador, Brazil, Argentina and Peru, were also analysed. Although phylogenetic analysis, amova analysis, the immanc assignment test and geneclass exclusion test analysis suggest that some of the medflies captured in California are derived from independent invasion events, analysis of specimens from the Los Angeles basin provides support for the hypothesis that an endemic population, probably derived from Guatemala, has been established.

Genetic Differentiation, Gene Flow and the Origin of Infestations of the Medfly, Ceratitis Capitata

The genetic structure of natural populations of the economically important dipteran species Ceratitis capitatawas analysed using both biochemical and molecular markers. This revealed considerable genetic variation in populations from different geographic regions. The nature of this variation suggests that the evolutionary history of the species involved the spread of individuals from the ancestral African populations through Europe and, more recently, to Latin America, Hawaii and Australia. The observed variation can be explained by various evolutionary forces acting differentially in the different geographic areas, including genetic drift, bottleneck effects, selection and gene flow. The analysis of the intrinsic variability of the medflys genome and the genetic relationships among populations of this pest is a prerequisite for any control programme.

On the origins of medfly invasion and expansion in Australia.

As a result of their rapid expansion and large larval host range, true fruit flies are among the worlds most important agricultural pest species. Among them, Ceratitis capitata has become a model organism for studies on colonization and invasion processes. The genetic aspects of the medfly invasion process have already been analysed throughout its range, with the exception of Australia. Bioinvasion into Australia is an old event: medfly were first captured in Australia in 1895, near Perth. After briefly appearing in Tasmania and the eastern states of mainland Australia, medfly had disappeared from these areas by the 1940s. Currently, they are confined to the western coastal region. South Australia seems to be protected from medfly infestations both by the presence of an inhospitable barrier separating it from the west and by the limited number of transport routes. However, numerous medfly outbreaks have occurred since 1946, mainly near Adelaide. Allele frequency data at 10 simple sequence repeat loci were used to study the genetic structure of Australian medflies, to infer the historical pattern of invasion and the origin of the recent outbreaks. The combination of phylogeographical analysis and Bayesian tests showed that colonization of Australia was a secondary colonization event from the Mediterranean basin and that Australian medflies were unlikely to be the source for the initial Hawaiian invasion. Within Australia, the Perth area acted as the core range and was the source for medfly bioinvasion in both Western and South Australia. Incipient differentiation, as a result of habitat fragmentation, was detected in some localized areas at the periphery of the core range.

Microsatellite analysis reveals remating by wild Mediterranean fruit fly females, Ceratitis capitata

Accurate estimates of remating in wild female insects are required for an understanding of the causes of variation in remating between individuals, populations and species. Such estimates are also of profound importance for major economic fruit pests such as the Mediterranean fruit fly (Ceratitis capitata). A major method for the suppression of this pest is the sterile insect technique (SIT), which relies on matings between mass‐reared, sterilized males and wild females. Remating by wild females will thus impact negatively on the success of SIT. We used microsatellite markers to determine the level of remating in wild (field‐collected) Mediterranean fruit fly females from the Greek Island of Chios. We compared the four locus microsatellite genotypes of these females and their offspring. Our data showed 7.1% of wild females remated. Skewed paternity among progeny arrays provided further evidence for double matings. Our lowest estimate of remating was 3.8% and the highest was 21%.

Microsatellite polymorphism in the Mediterranean fruit fly, Ceratitis capitata

A total of forty‐three simple sequence repeats (SSRs) were identified in the Mediterranean fruit fly (medfly) Ceratitis capitata. The most common SSR was the dinucleotide (TG)n/(CA)n occurring in thirty of the forty‐three microsatellite loci. Polymorphism at ten dinucleotide markers was investigated in 122 flies from six natural populations sampled in the native and colonized areas. A very high level of allelic diversity was detected in the species range. An average of 13.6 alleles was found over all the ten loci indicating the informativeness of SSRs as genetic markers for the medfly. The distribution of microsatellite polymorphism in the species range reflects the medfly colonization history.

Genetic variability and gene flow in geographical populations of Ceratitis capitata (Wied.) (medfly)

Two African populations of Ceratitis capitata (Kenya and Réunion Isl.) and two Mediterranean ones (Sardinia and Procida Isl.) have been studied for genetic variability at 25 loci by electrophoresis. Wright’s FST, Slatkin’s Nm* gene flow estimator, Nei’s distance (D) together with measures of variability such as [Hmacr ], [Pmacr ], Ā have been used to compare the population from Kenya with the other three. Parameters using gene frequencies (FST, D, Nm*) indicate the presence of substantial geographic heterogeneity, largely attributable to genetic drift and correlated with dispersion of the medfly from its source area (Subsaharan Africa) to the periphery. The Kenyan population has high genetic variability (assessed by [Hmacr ], [Pmacr ] and Ā), as might be expected given its native status. Significant gene flow estimates between Kenya and the derived Mediterranean populations supports the hypothesis of recent colonization. Part of the geographic heterogeneity is related to the presence of fixed alleles in the more differentiated Réunion population although it maintains the genetic attributes of the ancestral population. Selection or other forces may have played an important role in the differentiation of this population.

Population genetics of the potentially invasive African fruit fly species, Ceratitis rosa and Ceratitis fasciventris (Diptera: Tephritidae)

A set of 10 microsatellite markers was used to survey the levels of genetic variability and to analyse the genetic aspects of the population dynamics of two potentially invasive pest fruit fly species, Ceratitis rosa and C. fasciventris, in Africa. The loci were derived from the closely related species, C. capitata. The degree of microsatellite polymorphism in C. rosa and C. fasciventris was extensive and comparable to that of C. capitata. In C. rosa, the evolution of microsatellite polymorphism in its distribution area reflects the colonization history of this species. The mainland populations are more polymorphic than the island populations. Low levels of differentiation were found within the Africa mainland area, while greater levels of differentiation affect the islands. Ceratitis fasciventris is a central–east African species. The microsatellite data over the Uganda/Kenya spatial scale suggest a recent expansion and possibly continuing gene flow within this area. The microsatellite variability data from C. rosa and C. fasciventris, together with those of C. capitata, support the hypothesis of an east African origin of the Ceratitis spp.

Uncovering the tracks of a recent and rapid invasion: the case of the fruit fly pest Bactrocera invadens (Diptera: Tephritidae) in Africa.

Phytophagous insects of the genus Bactrocera are among the most economically important invasive fruit fly pests. In 2003, an unknown Bactrocera species was found in Kenya. First identified as an ‘aberrant form’ of the Asian B. dorsalis complex, it was later recognized as a new species, Bactrocera invadens. Within 2 years of its discovery, the species was recorded in several African countries, becoming an important quarantine pest. As this invasive fly was discovered only recently, no data are available on its invasion pattern in Africa. This pilot study attempts to infer from genetic data the dynamic aspects of the African invasion of this pest. Using microsatellite markers, we evaluated the level of genetic diversity and the extent of common ancestry among several African populations collected across the invaded areas. A sample from the Asian Sri Lankan population was analysed to confirm the Asian origin of this pest. Genetic data cast no doubt that Sri Lanka belongs to the native range, but only a small percentage of its genotypes can be found in Africa. African populations display relatively high levels of genetic diversity associated with limited geographical structure and no genetic footprints of bottlenecks. These features are indicative of processes of rapid population growth and expansion with possible multiple introductions. In the span of relatively few years, the African invasion registered the presence of at least two uncorrelated outbreaks, both starting from the East. The results of the analyses support that invasion started in East Africa, where B. invadens was initially isolated.