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

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.

Keywords: agricultural pests; general purpose genotype; polyphagy; prevalent invader genotype.

Figure 1

Geospatial distribution of combined genotypes of Naupactus cervinus for the Continental US (A) and the native range (B). Legend to the right lists all multilocus genotypes; pies indicate the relative presence of each multilocus genotype in each locality. Acronyms used for multilocus genotypes follow the nomenclature used by [19]. Localities are labeled according to codes in Table 1.

Figure 2

(A) Statistical parsimony network of mitochondrial haplotypes. Lines represent the most-parsimonious relationships between haplotypes and indicate one mutational step between two haplotypes. Dark green open circles represent individual haplotypes from the Forest Clade, light green open circles represent individual haplotypes from the Grassland Clade, red open circle represents the novel Y haplotype, and unlabeled black circles indicate inferred intermediate haplotypes not found in the samples. Rectangles indicate possible ancestral haplotypes. Circle size is proportional to haplotype frequency. (B) Statistical parsimony network of nuclear alleles and the graphical representation follows nomenclature explained in (A). Individual haplotype and allele codes follow Table 1A.