Out of the forest: past and present range expansion of a parthenogenetic weevil pest, or how to colonize the world successfully

Abstract

Previous research revealed complex diversification patterns in the parthenogenetic weevil Naupactus cervinus. To understand the origin of clonal diversity and successful spreading of this weevil, we investigated its geographic origin and possible dispersal routes and whether parthenogens can persist in habitats under unsuitable environmental conditions. This study is based on samples taken throughout a broad area of the species’ range. We used both mitochondrial and nuclear markers and applied phylogenetic and network analyses to infer possible relationships between haplotypes. Bayesian phylogeographic analyses and ecological niche modeling were used to investigate the processes that shaped genetic diversity and enabled the colonization of new geographic areas. Southeastern Brazil emerges as the original distribution area of N. cervinus. We detected two range expansions, one along natural corridors during the Pleistocene and the other in countries outside South America during recent times. Isolation due to climate shifts during the early Pleistocene led to diversification in two divergent clades, which probably survived in different refugia of the Paranaense Forest and the Paraná River delta. The origin of the clonal diversity was probably a complex process including mutational diversification, hybridization, and secondary colonization. The establishment of N. cervinus in areas outside its native range may indicate adaptation to drier and cooler conditions. Parthenogenesis would be advantageous for the colonization of new environments by preventing the breakup of successful gene combinations. As in other insect pests, the present distribution of N. cervinus results from both its evolutionary history and its recent history related to human activities.

Phylogeny of the tribe Naupactini (Coleoptera: Curculionidae) based on morphological characters

“…However, additional morphological evidence for other species of Naupactus , and preliminar molecular analyses based on a large taxon sampling suggest that N. cervinus and N. leucoloma belong to different species groups of this genus (Lanteri & Marvaldi, ; Scataglini et al ., ; M. Rodriguero et al ., unpublished data). Aramigus tessellatus , N. cervinus and N. leucoloma are derived lineages of the Pantomorus–Naupactus complex sensu Buchanan () which have accumulated several apomorphic characters, among them reduction of humeri and hindwings and parthenogenetic reproduction (Normark & Lanteri, ; Guzmán et al ., ; Rodriguero et al ., , ).…”

The Effect of Reproductive System on Invasiveness: Lessons from South American Weevils

“…The South American tribe Naupactini comprises numerous parthenogenetic species of economic importance as pests that invaded other continents (Lanteri & Normark 1995), among which are the "Fuller's rose weevil" Naupactus cervinus Boheman (Coleoptera: Curculionidae), and the white-fringed weevil, Naupactus leucoloma Boheman (Coleoptera: Curculionidae) (Guzmán et al 2012;Lanteri et al 2013;Rodriguero et al 2016). These species have unisexual lineages, as rearing experiments and population sex ratios suggested (Buchanan 1939;Lanteri & Normark 1995).…”

Potential Geographic Distributions of Two Parthenogenetic Weevils (Coleoptera: Curculionidae) Associated with Citrus in Argentina and Brazil

“…Southeastern USA (Florida), southern Africa, and eastern Australia are suitable for all the parthenogenetic Naupactini previously studied, and central Europe is suitable for most of them (e.g., A. taeniatulus, F. sordidus, E. fallax, and Naupactus cervinus Boheman (all Coleoptera: Curculionidae) [Lanteri et al 2013b;Rodriguero et al 2016]). The predicted suitable areas for P. cinerosus are similar to those for the latter species, while that for P. fluctuosus is even broader.…”

“…Despite the fact that P. fluctuosus and P. cinerosus may reproduce parthenogenetically, and that our models predict several of the surveyed areas (in South America and worldwide) as suitable for both species, neither of them is known to occur overseas. Indeed, only 8 of more than 30 parthenogenetic Naupactini species native to Argentina and Brazil have established populations far from their original distribution areas, the most widespread being the "fuller's rose weevil" N. cervinus, a serious pest of citrus and many other crops (Lanteri et al 2002a, b;Guedes et al 2005;Rodriguero et al 2016).…”

“…This research project was supported by Universidad Nacional de La Plata (UNLP), Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT), and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), through grants CONICET-IBOL 2318/11, BID-PICT 2012/2524, 2016/2798, 2016…”