Dominique Mazzi

Molecular genetics and genomics generate new insights into invertebrate pest invasions.

Invertebrate pest invasions and outbreaks are associated with high social, economic, and ecological costs, and their significance will intensify with an increasing pressure on agricultural productivity as a result of human population growth and climate change. New molecular genetic and genomic techniques are available and accessible, but have been grossly underutilized in studies of invertebrate pest invasions, despite that they are useful tools for applied pest management and for understanding fundamental features of pest invasions including pest population demographics and adaptation of pests to novel and/or changing environments. Here, we review current applications of molecular genetics and genomics in the study of invertebrate pest invasions and outbreaks, and we highlight shortcomings from the current body of research. We then discuss recent conceptual and methodological advances in the areas of molecular genetics/genomics and data analysis, and we highlight how these advances will further our understanding of the demographic, ecological, and evolutionary features of invertebrate pest invasions. We are now well equipped to use molecular data to understand invertebrate dispersal and adaptation, and this knowledge has valuable applications in agriculture at a time when these are critically required.

MALE COURTSHIP SONG AND FEMALE PREFERENCE VARIATION BETWEEN PHYLOGEOGRAPHICALLY DISTINCT POPULATIONS OF DROSOPHILA MONTANA

Abstract Understanding the variation within and between populations in important male mating traits and female preferences is crucial to theories concerning the origin of sexual isolation by coevolution or other processes. There have been surprisingly few studies on the extent of variation and covariation within and between populations, especially where the evolutionary relationships between populations are understood. Here we examine variation in female preferences and a sexually selected male song trait, the carrier frequency of the song, within and between populations from different phylogeographic clusters of Drosophila montana. Song is obligatory for successful mating in this species, and both playback and field studies implicate song carrier frequency as the most important parameter in male song. Carrier frequency varied among three recently collected populations from Oulanka (Finland), Vancouver (Canada), and Colorado (central United States), which represent the main phylogeographic groups in D. montana. Males from Colorado had the most distinct song frequency, which did not follow patterns of genetic differentiation. There was considerable variation in preference functions within, and some variation between, populations. Surprisingly, females from three lines from Colorado seem to have preferences disfavoring the extreme male trait found in this population. We discuss sources of selection on male song and female preference.

Worldwide population genetic structure of the oriental fruit moth (Grapholita molesta), a globally invasive pest

BackgroundInvasive pest species have large impacts on agricultural crop yields, and understanding their population dynamics is important for ensuring food security. The oriental fruit moth Grapholita molesta is a cosmopolitan pest of stone and pome fruit species including peach and apple, and historical records indicate that it has invaded North and South America, Europe, Australia and Africa from its putative native range in Asia over the past century.ResultsWe used 13 microsatellite loci, including nine newly developed markers, to characterize global population structure of G. molesta. Approximately 15 individuals from each of 26 globally distributed populations were genotyped. A weak but significant global pattern of isolation-by-distance was found, and G. molesta populations were geographically structured on a continental scale. Evidence does not support that G. molesta was introduced to North America from Japan as previously proposed. However, G. molesta was probably introduced from North America to The Azores, South Africa, and Brazil, and from East Asia to Australia. Shared ancestry was inferred between populations from Western Europe and from Brazil, although it remains unresolved whether an introduction occurred from Europe to Brazil, or vice versa. Both genetic diversity and levels of inbreeding were surprisingly high across the range of G. molesta and were not higher or lower overall in introduced areas compared to native areas. There is little evidence for multiple introductions to each continent (except in the case of South America), or for admixture between populations from different origins.ConclusionsCross-continental introductions of G. molesta appear to be infrequent, which is surprising given its rapid worldwide expansion over the past century. We suggest that area-wide spread via transport of fruits and other plant materials is a major mechanism of ongoing invasion, and management efforts should therefore target local and regional farming communities and distribution networks.

No Need to Discriminate? Reproductive Diploid Males in a Parasitoid with Complementary Sex Determination

Diploid males in hymenopterans are generally either inviable or sterile, thus imposing a severe genetic load on populations. In species with the widespread single locus complementary sex determination (sl-CSD), sex depends on the genotype at one single locus with multiple alleles. Haploid (hemizygous) individuals are always males. Diploid individuals develop into females when heterozygous and into males when homozygous at the sex determining locus. Our comparison of the mating and reproductive success of haploid and diploid males revealed that diploid males of the braconid parasitoid Cotesia glomerata sire viable and fertile diploid daughters. Females mated to diploid males, however, produced fewer daughters than females mated to haploid males. Nevertheless, females did not discriminate against diploid males as mating partners. Diploid males initiated courtship display sooner than haploid males and were larger in body size. Although in most species so far examined diploid males were recognized as genetic dead ends, we present a second example of a species with sl-CSD and commonly occurring functionally reproductive diploid males. Our study suggests that functionally reproductive diploid males might not be as rare as hitherto assumed. We argue that the frequent occurrence of inbreeding in combination with imperfect behavioural adaptations towards its avoidance promote the evolution of diploid male fertility.

Structured populations of the oriental fruit moth in an agricultural ecosystem.

Intercontinental trade has led to multiple introductions of invasive pest species at a global scale. Molecular analyses of the structure of populations support the understanding of ecological strategies and evolutionary patterns that promote successful biological invasions. The oriental fruit moth, Grapholita (=Cydia) molesta, is a cosmopolitan and economically destructive pest of stone and pome fruits, expanding its distribution range concomitantly with global climate warming. We used ten newly developed polymorphic microsatellite markers to examine the genetic structure of G. molesta populations in an agricultural ecosystem in the Emilia‐Romagna region of northern Italy. Larvae collected in eight sampling sites were assigned to a mosaic of five populations with significant intra‐regional structure. Inferred measures of gene flow within populations implicated both active dispersal, and passive dispersal associated with accidental anthropogenic displacements. Small effective population sizes, coupled with high inbreeding levels, highlighted the effect of orchard management practices on the observed patterns of genetic variation within the sampling sites. Isolation by distance did not appear to play a major role at the spatial scale considered. Our results provide new insights into the population genetics and dynamics of an invasive pest species at a regional scale.

Inbreeding in a natural population of the gregarious parasitoid wasp Cotesia glomerata.

Inbreeding occurs in numerous animal and plant species. In haplodiploid hymenopterans with the widespread single locus complementary sex determination, the frequency of diploid males, which are produced at the expense of females, is increased under inbreeding. Diploid males in species of bees, ants and wasps are typically either unviable or effectively sterile and thus impose a severe genetic load on populations. However, a recent study indicated that diploid males can be reproductive in the gregarious parasitoid wasp Cotesia glomerata, effectively reducing the diploid male load. To understand the role of inbreeding as a potential selective pressure towards the evolution of diploid male fertility, we genotyped specimens collected in the field at four locations using microsatellite markers to estimate the ratio of sibling matings under natural conditions. Results show that more than half of all matings involved siblings. We argue that the frequent occurrence of inbreeding has driven the evolution of diploid male fertility.

Stay cool, travel far: cold‐acclimated oriental fruit moth females have enhanced flight performance but lay fewer eggs

Acclimation to a particular environment may provide organisms with advantages in that environment. In species with multiple generations per year, acclimation may cause life‐history traits to vary with season and between generations. We investigated flight performance, lifetime egg production, and longevity in relation to the temperature experienced during development and adulthood in the invasive moth pest Grapholita molesta (Busck) (Lepidoptera: Tortricidae). We found that females that developed at low temperature had good flight abilities when they were flown at low, intermediate, and high temperatures. At high temperature, females that developed at high temperature did not outperform females that developed at low temperature. Flight performance was generally poor at low ambient temperature. Our findings suggest a beneficial acclimation effect, occurring at low temperature. Nonetheless, there were potential costs of development at low temperature: development took longer, resulting in smaller females, which laid fewer eggs. Given temporal and spatial temperature variability in the field, dispersal potential should not be considered homogeneous within populations or across generations. Our results suggest that the most favourable time periods for female dispersal are at the beginning and towards the end of the host crop growing season, which has potential implications for monitoring the occurrence and range expansion of this invasive pest species.

Cross-generational effects of temperature on flight performance, and associated life-history traits in an insect

Nongenetic parental effects may affect offspring phenotype, and in species with multiple generations per year, these effects may cause life‐history traits to vary over the season. We investigated the effects of parental, offspring developmental and offspring adult temperatures on a suite of life‐history traits in the globally invasive agricultural pest Grapholita molesta. A low parental temperature resulted in female offspring that developed faster at low developmental temperature compared with females whose parents were reared at high temperature. Furthermore, females whose parents were reared at low temperature were heavier and more fecund and had better flight abilities than females whose parents were reared at high temperature. In addition to these cross‐generational effects, females developed at low temperature had similar flight abilities at low and high ambient temperatures, whereas females developed at high temperature had poorer flight abilities at low than at high ambient temperature. Our findings demonstrate a pronounced benefit of low parental temperature on offspring performance, as well as between‐ and within‐generation effects of acclimation to low temperature. In cooler environments, the offspring generation is expected to develop more rapidly than the parental generation and to comprise more fecund and more dispersive females. By producing phenotypes that are adaptive to the conditions inducing them as well as heritable, cross‐generational plasticity can influence the evolutionary trajectory of populations. The potential for short‐term acclimation to low temperature may allow expanding insect populations to better cope with novel environments and may help to explain the spread and establishment of invasive species.

No evidence for increased extinction proneness with decreasing effective population size in a parasitoid with complementary sex determination and fertile diploid males

BackgroundIn species with single locus complementary sex determination (sl-CSD), the sex of individuals depends on their genotype at one single locus with multiple alleles. Haploid individuals are always males. Diploid individuals are females when heterozygous, but males when homozygous at the sex-determining locus. Diploid males are typically unviable or effectively sterile, hence imposing a genetic load on populations. Diploid males are produced from matings of partners that share an allele at the sex-determining locus. The lower the allelic diversity at the sex-determining locus, the more diploid males are produced, ultimately impairing the growth of populations and jeopardizing their persistence. The gregarious endoparasitoid wasp Cotesia glomerata is one of only two known species with sl-CSD and fertile diploid males.ResultsBy manipulating the relatedness of the founders, we established replicated experimental populations of the parasitoid C. glomerata differing in their genetic effective size, and thus in allelic richness at the sex-determining locus and in the expected magnitude of diploid male production. Our long-term survey of population welfare and persistence did not provide evidence for increased proneness to population extinction with decreasing initial genetic effective population size. Most recorded surrogates of fitness nevertheless decayed over time and most experimental populations eventually went extinct, suggesting that the negative effects of inbreeding outweighed any premium from the fertility of diploid males.ConclusionsThe fertility of diploid males may have evolved as an adaptation prompted by the risk of extinction looming over small isolated populations of species with sl-CSD. However, fertility of diploid males does not negate the costs imposed by their production, and although it may temporarily stave off extinction, it is not sufficient to eradicate the negative effects of inbreeding.

Ladies last: diel rhythmicity of adult emergence in a parasitoid with complementary sex determination

Protandry, the earlier adult emergence of males, is explained as either an adaptive strategy maximizing male mating opportunities at the same time as minimizing female pre‐reproductive mortality, or as an incidental by‐product of sexual dimorphism fuelled by selection for other life‐history traits. Adult emergence sequences are monitored of broods of the gregarious larval endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) undergoing pupal development under different temperature regimes. As a haplodiploid species with single‐locus complementary sex determination, gender in C. glomerata is determined by the genotype at one sex locus. Haploids are always male, whereas diploids are female when heterozygous but male when homozygous at the sex locus. Sibling mating promotes homozygosity and thus the production of diploid males. Diploid males are produced at the expense of females, and impose a genetic burden on individuals and populations, despite their exceptional fertility in C. glomerata. Emergence of broods is typically completed within 2 days. Irrespective of temperature, males emerge earlier and within a shorter time interval than females, and a majority of the males in a cluster emerge before the first female. The implications of an incomplete temporal segregation of the sexes on the incidence of inbreeding in C. glomerata are discussed in the light of its sex determination mechanism and its patterns of mating, host exploitation and natal dispersal.