Mito-nuclear genetic comparison in a Wolbachia infected weevil: insights on reproductive mode, infection age and evolutionary forces shaping genetic variation

<p>Abstract</p> <p>Background</p> <p>Maternally inherited endosymbionts like <it>Wolbachia pipientis </it>are in linkage disequilibrium with the mtDNA of their hosts. Therefore, they can induce selective sweeps, decreasing genetic diversity over many generations. This sex ratio distorter, that is involved in the origin of parthenogenesis and other reproductive alterations, infects the parthenogenetic weevil <it>Naupactus cervinus</it>, a serious pest of ornamental and fruit plants.</p> <p>Results</p> <p>Molecular evolution analyses of mitochondrial (<it>COI</it>) and nuclear (<it>ITS1</it>) sequences from 309 individuals of <it>Naupactus cervinus </it>sampled over a broad range of its geographical distribution were carried out. Our results demonstrate lack of recombination in the nuclear fragment, non-random association between nuclear and mitochondrial genomes and the consequent coevolution of both genomes, being an indirect evidence of apomixis. This weevil is infected by a single <it>Wolbachia </it>strain, which could have caused a moderate bottleneck in the invaded population which survived the initial infection.</p> <p>Conclusions</p> <p>Clonal reproduction and <it>Wolbachia </it>infection induce the coevolution of bacterial, mitochondrial and nuclear genomes. The time elapsed since the <it>Wolbachia </it>invasion would have erased the traces of the demographic crash in the mtDNA, being the nuclear genome the only one that retained the signal of the bottleneck. The amount of genetic change accumulated in the mtDNA and the high prevalence of <it>Wolbachia </it>in all populations of <it>N. cervinus </it>agree with the hypothesis of an ancient infection. <it>Wolbachia </it>probably had great influence in shaping the genetic diversity of <it>N. cervinus</it>. However, it would have not caused the extinction of males, since sexual and asexual infected lineages coexisted until recent times.</p

Mito-nuclear genetic comparison in a Wolbachia infected weevil: Insights on reproductive mode, infection age and evolutionary forces shaping genetic variation

Background: Maternally inherited endosymbionts like Wolbachia pipientis are in linkage disequilibrium with the mtDNA of their hosts. Therefore, they can induce selective sweeps, decreasing genetic diversity over many generations. This sex ratio distorter, that is involved in the origin of parthenogenesis and other reproductive alterations, infects the parthenogenetic weevil Naupactus cervinus, a serious pest of ornamental and fruit plants. Results: Molecular evolution analyses of mitochondrial (COI) and nuclear (ITS1) sequences from 309 individuals of Naupactus cervinus sampled over a broad range of its geographical distribution were carried out. Our results demonstrate lack of recombination in the nuclear fragment, non-random association between nuclear and mitochondrial genomes and the consequent coevolution of both genomes, being an indirect evidence of apomixis. This weevil is infected by a single Wolbachia strain, which could have caused a moderate bottleneck in the invaded population which survived the initial infection. Conclusions: Clonal reproduction and Wolbachia infection induce the coevolution of bacterial, mitochondrial and nuclear genomes. The time elapsed since the Wolbachia invasion would have erased the traces of the demographic crash in the mtDNA, being the nuclear genome the only one that retained the signal of the bottleneck. The amount of genetic change accumulated in the mtDNA and the high prevalence of Wolbachia in all populations of N. cervinus agree with the hypothesis of an ancient infection. Wolbachia probably had great influence in shaping the genetic diversity of N. cervinus. However, it would have not caused the extinction of males, since sexual and asexual infected lineages coexisted until recent times.Facultad de Ciencias Naturales y Muse

The effect of reproductive system on invasiveness: lessons from South American weevils

Successful invasion of a species into novel, marginal areas often requires the ability to face different ecological characteristics than those prevailing in its native environment. In insects, one of the factors that affect invasiveness is the reproductive system. Unisexuality provides advantages because a single specimen can initiate a new population. Unisexual reproduction precludes breakup of genetic combinations that promote ecological specialization, although it may limit evolutionary potential for colonization. In order to assess the importance of the reproductive mode in the colonization ability of the weevils that are native to South America, we compared 1 bisexual and 2 parthenogenetic species that expanded their ranges in the last 2 centuries. First, for parthenogenetic species we tested clonality of the sample. Second, we proposed central and marginal areas through phylogeographic and habitat modeling analyses, and identified the pathways of dispersal for each species. Bisexual Naupactus xanthographus (Germar) (Coleoptera: Curculionidae) expanded its range westward to areas with similar environmental constraints than in its native ecosystem. Conversely, parthenogenetic Naupactus leucoloma Boheman and Naupactus cervinus Boheman (both Coleoptera: Curculionidae) invaded other continents where they had low to null predicted habitat suitability. While a single clone of N. cervinus successfully established around the world in areas with apparently adverse conditions, clones of N. leucoloma expanded their range to areas only moderately suitable. We conclude that parthenogenesis is a driver in these particular species for colonization of marginal habitats. However, N. cervinus also would have pre-existing adaptations that allowed it to establish in areas with apparently low potential to surviveLa colonización de áreas marginales a menudo requiere que la especie invasora sea capaz de enfrentar características ecológicas diferentes a aquellas que predominan en su área nativa. En los insectos, uno de los factores que afectan la capacidad invasiva figura el sistema reproductivo. La unisexualidad proporciona varias ventajas, entre ellas la capacidad de fundar una nueva población a partir de un único especimen y evitar la ruptura de las combinaciones genéticas que promueven la especialización ecológica, esta última puede limitar el potencial evolutivo para la colonización. A fin de evaluar la importancia del modo reproductivo en la capacidad colonizadora de un grupo de gorgojos nativos de Sudamérica, comparamos dos especies con reproducción partenogenética y una especie bisexual que expandieron su rango geográfico a lo largo de los últimos 200 años. Por un lado, para las especies partenogenéticas pusimos a prueba la hipótesis de reproducción clonal. Además, propusimos áreas centrales y marginales a través de análisis filogeográficos y de modelado ecológico del hábitat e identificamos las rutas de dispersión de cada especie. La especie bisexual Naupactus xanthographus (Germar) (Coleoptera: Curculionidae) expandió su rango hacia el oeste, estableciéndose en áreas con restricciones ambientales similares a las de su área nativa. Por el contrario, las especies partenogenéticas Naupactus leucoloma Boheman y Naupactus cervinus Boheman (ambos Coleoptera: Curculionidae) invadieron otros continentes, donde las predicciones de ocurrencia en base a las condiciones del hábitat son bajas a nulas. Un único clon de N. cervinus consiguió establecerse en áreas con condiciones aparentemente adversas y los clones de N. leucoloma solo expandieron su rango a áreas moderadamente adecuadas. Concluimos que la partenogénesis es un factor fundamental en la colonización exitosa de hábitats marginales de estos gorgojos. Sin embargo, N. cervinus tendría adaptaciones pre-existentes que le habrían permitido el establecimiento en áreas con un potencial aparentemente bajo para la supervivencia.Facultad de Ciencias Naturales y Muse

A tale of swinger insects: signatures of past sexuality between divergent lineages of a parthenogenetic weevil revealed by ribosomal intraindividual variation

Naupactus cervinus (Boheman) (Curculionidae, Naupactini) is a parthenogenetic weevil native to the Paranaense Forest which displays high levels of genetic variation. Two divergent clades were identified, one ranging in forest areas (Forest clade), and the other in open vegetation areas (Grassland clade). Both of them have individuals with high levels of heterozygosity in ribosomal sequences. Investigation of intraindividual variation in ITS1 sequences through cloning and posterior sequencing suggested that mating between both groups most likely occurred in the Paranaense Forest after a secondary contact, which led to fixed heterozygotes as a consequence of parthenogenesis. Otherwise, sexual segregation would have disrupted multilocus genotypes. Only a small number of heterozygous genotypes of all the possible combinations are found in nature. We propose the occurrence of a hybrid zone in the Paranaense Forest. The fact that it is one of the most important biodiversity hotspots of the world, together with its key role for investigating evolutionary processes, makes it worthy of conservation. This is the first genetic evidence of bisexuality in N. cervinus.Facultad de Ciencias Naturales y Muse

Stable inversion clines in a grasshopper species group despite complex geographical history

Chromosomal inversions are known to play roles in adaptation and differentiation in many species. They involve clusters of correlated genes (i.e., loci in linkage disequilibrium, LD) possibly associated with environmental variables. The grasshopper "species complex" Trimerotropis pallidipennis comprises several genetic lineages distributed from North to South America in arid and semi-arid high-altitude environments. The southernmost lineage, Trimerotropis sp., segregates for four to seven putative inversions that display clinal variation, possibly through adaptation to temperate environments. We analysed chromosomal, mitochondrial and genome-wide single nucleotide polymorphism data in 19 Trimerotropis sp. populations mainly distributed along two altitudinal gradients (MS and Ju). Populations across Argentina comprise two main chromosomally and genetically differentiated lineages: one distributed across the southernmost border of the "Andes Centrales," adding evidence for a differentiation hotspot in this area; and the other widely distributed in Argentina. Within the latter, network analytical approaches to LD found three clusters of correlated loci (LD-clusters), with inversion karyotypes explaining >79% of the genetic variation. Outlier loci associated with environmental variables mapped to two of these LD-clusters. Furthermore, despite the complex geographical history indicated by population genetic analyses, the clines in inversion karyotypes have remained stable for more than 20 generations, implicating their role in adaptation and differentiation within this lineage. We hypothesize that these clines could be the consequence of a coupling between extrinsic postzygotic barriers and spatially varying selection along environmental gradients resulting in a hybrid zone. These results provide a framework for future investigations about candidate genes implicated in rapid adaptation to new environments.Peer reviewe

Host-specific gene expression as a tool for introduction success in <i>Naupactus</i> parthenogenetic weevils

Food resource access can mediate establishment success in invasive species, and generalist herbivorous insects are thought to rely on mechanisms of transcriptional plasticity to respond to dietary variation. While asexually reproducing invasives typically have low genetic variation, the twofold reproductive capacity of asexual organisms is a marked advantage for colonization. We studied host-related transcriptional acclimation in parthenogenetic, invasive, and polyphagous weevils: Naupactus cervinus and N. leucoloma. We analyzed patterns of gene expression in three gene categories that can mediate weevil-host plant interactions through identification of suitable host plants, short-term acclimation to host plant defenses, and long-term adaptation to host plant defenses and their pathogens. This approach employed comparative transcriptomic methods to investigate differentially expressed host detection, detoxification, immune defense genes, and pathway-level gene set enrichment. Our results show that weevil gene expression responses can be host plant-specific, and that elements of that response can be transgenerational. Some host plant groups, such as legumes, appear to be more taxing as they elicit a complex gene expression response which is both strong in intensity and specific in identity. However, the weevil response to taxing host plants shares many differentially expressed genes with other stressful situations, such as host plant cultivation conditions and transition to novel host, suggesting that there is an evolutionarily favorable shared gene expression regime for responding to different types of stressful situations. Modulating gene expression in the absence of other avenues for phenotypic adaptation may be an important mechanism of successful colonization for these introduced insects.Facultad de Ciencias Naturales y Muse

Evolutionary history of the little fire ant Wasmannia auropunctata before global invasion: Inferring dispersal patterns, niche requirements and past and present distribution within its native range

The evolutionary history of invasive species within their native range may involve key processes that allow them to colonize new habitats. Therefore, phylogeographic studies of invasive species within their native ranges are useful to understand invasion biology in an evolutionary context. Here we integrated classical and Bayesian phylogeographic methods using mitochondrial and nuclear DNA markers with a palaeodistribution modelling approach, to infer the phylogeographic history of the invasive ant Wasmannia auropunctata across its native distribution in South America. We discuss our results in the context of the recent establishment of this mostly tropical species in the Mediterranean region. Our Bayesian phylogeographic analysis suggests that the common ancestor of the two main clades of W. auropunctata occurred in central Brazil during the Pliocene. Clade A would have differentiated northward and clade B southward, followed by a secondary contact beginning about 380 000 years ago in central South America. There were differences in the most suitable habitats among clades when considering three distinct climatic periods, suggesting that genetic differentiation was accompanied by changes in niche requirements, clade A being a tropical lineage and clade B a subtropical and temperate lineage. Only clade B reached more southern latitudes, with a colder climate than that of northern South America. This is concordant with the adaptation of this originally tropical ant species to temperate climates prior to its successful establishment in the Mediterranean region. This study highlights the usefulness of exploring the evolutionary history of invasive species within their native ranges to better understand biological invasions. © 2016 European Society for Evolutionary Biology

Wolbachia, una pandemia con posibilidades

La infección causada por Wolbachia es la más extendida entre los animales. La capacidad de esta bacteria para manipular la reproducción de sus hospedadores la posicionan en el centro de la biología de los organismos, influyendo en procesos tan capitales como la determinación del sexo, el ciclo celular, la formación y extinción de especies y el comportamiento de artrópodos entre los que se cuentan varias plagas y vectores de enfermedades. Cualidades tales como la herencia vertical de Wolbachia, la velocidad a la que se propaga en las poblaciones que afecta, la capacidad de bloquear la actividad patogénica de diversos microorganismos o de acortar el ciclo de vida de sus hospedadores la señalan como un potencial instrumento para el control de poblaciones de insec - tos y nematodos perjudiciales. ¿Cuáles son las posibilidades que nos ofrece esta pandemia? En la presente contribución se presenta una revisión de los aspectos fundamen - tales de esta infección y sus implicancias prácticas para el manejo de insectos plaga. Esta revisión está basada en el simposio del mismo nombre acontecido en el VIII Congreso Argentino de Entomología

Molecular and Morphological Phylogenetic Analysis of Naupactus Dejean (Curculionidae: Entiminae) and Allied Genera: The Dilemma of Classification

Naupactus (Curculionidae: Entiminae) is the most speciose weevil genus of the tribe Naupactini. The main objective of this work is to recognize species groups within Naupactus and to analyze the relationships between this and other Neotropical genera. For this purpose, we compiled a combined data matrix of 60 terminal units corresponding to 40 species for which we recorded 812 molecular and morphological characters (763 and 49 respectively), which were analyzed by Maximum Parsimony and Bayesian analyses. The single tree obtained from each analysis was rooted with Cyrtomon inhalatus. The species of Naupactus were recovered as different monophyletic groups, some of them closer to other genera of Naupactini (Lanterius, Teratopactus, Pantomorus and Parapantomorus) than to species of the same genus. We conclude that Naupactus is non-monophyletic, even though most species can be recognized based on a particular combination of morphological characters, which are probably symplesiomorphic. To be consistent with the cladistic principles, some genera diversified in marginal areas of the Pantomorus-Naupactus complex should be synonymized with Naupactus; however, these nomenclatural changes may not ensure a generic definition based on synapomorphies. We prefer to be conservative about the current classification until more evidence is available. The only nomenclatural amendments proposed herein are the transference of Naupactus inermis Hustache to Lanterius and of N. setarius to Symmathetes

Biological characterization of Aedes albopictus (Diptera: Culicidae) in Argentina: implications for arbovirus transmission

Abstract Aedes albopictus (Diptera: Culicidae) is an invasive mosquito, native to Asia, that has expanded its range worldwide. It is considered to be a public health threat as it is a competent vector of viruses of medical importance, including dengue, chikungunya, and Zika. Despite its medical importance there is almost no information on biologically important traits of Ae. albopictus in Argentina. We studied life cycle traits, demographic parameters and analyzed the competence of this mosquito as a virus vector. In addition, we determined the prevalence of Wolbachia strains in Ae. albopictus as a first approach to investigate the potential role of this bacteria in modulating vector competence for arboviruses. We observed low hatch rates of eggs, which led to a negative growth rate. We found that Ae. albopictus individuals were infected with Wolbachia in the F1 but while standard superinfection with wAlbA and wAlbB types was found in 66.7% of the females, 16.7% of the females and 62.5% of the males were single-infected with the wAlbB strain. Finally, despite high levels of infection and dissemination, particularly for chikungunya virus, Ae. albopictus from subtropical Argentina were found to be relatively inefficient vectors for transmission of both chikungunya and dengue viruses