Genetically Depauperate and Still Successful: Few Multilocus Genotypes of the Introduced Parthenogenetic Weevil Naupactus cervinus (Coleoptera: Curculionidae) Prevail in the Continental United States

SIMPLE SUMMARY: The Fuller’s rose weevil Naupactus cervinus has become a globally invasive pest of several ornamental plants and fruit trees. This weevil has caused severe economic losses, and eggs laid on fruit are a quarantine barrier for several countries’ exports of fruit to markets in East Asia. Previous studies revealed that a genotype with high colonization ability successfully expanded throughout most continents, even in areas of inadequate environmental conditions, where this insect performs unexpectedly well, and that parthenogenesis may have helped to expand its geographic range. Pre-existing variation might have been eroded either by natural selection, leading to fixation of this variant able to cope with different environmental conditions to those in the native range, or by repeated bottlenecks during the process of invasion. To better understand the ecology of this invasive pest, we enlarged the sampling in areas of introduction, such as the southern United States, and surveyed genetic variation through mitochondrial and nuclear sequences in 13 localities across three states. Our results indicate that the invader genotype, already identified, has also colonized the continental United States (US), supporting the hypothesis of a general-purpose genotype capable of coping with adverse conditions and enlarging its geographical range. Parthenogenesis, and its associated lack of recombination, may help in maintaining a general-purpose genotype that facilitates the colonization of distant, unsuitable areas. However, demographic advantages linked to parthenogenesis as the sole mode of reproduction are also possible. ABSTRACT: Naupactus cervinus is a parthenogenetic weevil native to South America that is currently distributed worldwide. This flightless species is polyphagous and capable of modifying gene expression regimes for responding to stressful situations. Naupactus cervinus was first reported in the continental United States in 1879 and has rapidly colonized most of the world since. Previous studies suggested that an invader genotype successfully established even in areas of unsuitable environmental conditions. In the present work, we analyze mitochondrial and nuclear sequences from 71 individuals collected in 13 localities across three states in the southern US, in order to describe the genetic diversity in this area of introduction that has not yet been previously studied. Our results suggest that 97% of the samples carry the most prevalent invader genotype already reported, while the rest shows a close mitochondrial derivative. This would support the hypothesis of a general purpose genotype, with parthenogenesis and its associated lack of recombination maintaining the linkage of genetic variants capable of coping with adverse conditions and enlarging its geographical range. However, demographic advantages related to parthenogenetic reproduction as the main driver of geographic expansion (such as the foundation of a population with a single virgin female) cannot be ruled out. Given the historical introduction records and the prevalence of the invader genotype, it is possible that the continental US may act as a secondary source of introductions to other areas. We propose that both the parthenogenesis and scarce genetic variation in places of introduction may, in fact, be an asset that allows N. cervinus to thrive across a range of environmental conditions.