Abstract

BackgroundSome of the most important malaria vectors in South America belong to the Albitarsis Complex (Culicidae; Anophelinae; Anopheles). Understanding the origin, nature, and geographical distribution of species diversity in this important complex has important implications for vector incrimination, control, and management, and for modelling future responses to climate change, deforestation, and human population expansion. This study attempts to further explore species diversity and evolutionary history in the Albitarsis Complex by undertaking a characterization and phylogenetic analysis of the mitogenome of all 10 putative taxa in the Albitarsis Complex.MethodsMitogenome assembly and annotation allowed for feature comparison among Albitarsis Complex and Anopheles species. Selection analysis was conducted across all 13 protein-coding genes. Maximum likelihood and Bayesian inference methods were used to construct gene and species trees, respectively. Bayesian methods were also used to jointly estimate species delimitation and species trees.ResultsGene composition and order were conserved across species within the complex. Unique signatures of positive selection were detected in two species—Anopheles janconnae and An. albitarsis G—which may have played a role in the recent and rapid diversification of the complex. The COI gene phylogeny does not fully recover the mitogenome phylogeny, and a multispecies coalescent-based phylogeny shows that considerable uncertainty exists through much of the mitogenome species tree. The origin of divergence in the complex dates to the Pliocene/Pleistocene boundary, and divergence within the distinct northern South American clade is estimated at approximately 1 million years ago. Neither the phylogenetic trees nor the delimitation approach rejected the 10-species hypothesis, although the analyses could not exclude the possibility that four putative species with scant a priori support (An. albitarsis G, An. albitarsis H, An. albitarsis I, and An. albitarsis J), represent population-level, rather than species-level, splits.ConclusionThe lack of resolution in much of the species tree and the limitations of the delimitation analysis warrant future studies on the complex using genome-wide data and the inclusion of additional specimens, particularly from two putative species, An. albitarsis I and An. albitarsis J.Graphical

Highlights

  • Some of the most important malaria vectors in South America belong to the Albitarsis Complex (Culici‐ dae; Anophelinae; Anopheles)

  • These specimens have been stored as vouchers or had their DNA stored in archive collections of the Walter Reed Biosystematics Unit (WRBU), Smithsonian Institution–National Museum of Natural History, Museum Support Center (MSC), Suitland, Maryland, USA, or in the frozen tissue collection at the Natural History Museum, London, UK

  • Population size parameter (θ) was assigned an inverse-gamma prior run for different values: IG(3, 0.005), IG(3, 0.01), and IG(3, 0.02), i.e., IG(α, β), giving a mean of m = β/(α − 1), or mean species nucleotide diversity of 0.25, 0.,5 and 1.0%. We considered these to be a realistic range of estimates for diversity in the Albitarsis Complex, where mean nucleotide diversity among species was estimated at 0.87%, based on c oxidase I (COI) barcodes sequenced in Motoki et al [11]

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Summary

Introduction

Some of the most important malaria vectors in South America belong to the Albitarsis Complex (Culici‐ dae; Anophelinae; Anopheles). Five species of Plasmodium cause malaria in humans [3, 4], but two—Plasmodium falciparum and Plasmodium vivax— are considered the greatest threat The former is the predominant species in Africa, where almost 95% of global malaria cases and deaths occur, while the latter predominates in the Americas, accounting for 75% of the approximately 1 million cases reported annually [2]. The importance of An. marajoara in Plasmodium transmission in the Brazilian Amazon is comparable to that of An. darlingi in established forest settlements [12], while it has been found to be the most important malaria vector at emerging frontier settlements [13]. Many of the species in the complex, including An. marajoara and An. deaneorum, are predicted to expand their distributions due to the effects of climate change and are likely to be of increasing public health importance in the future [26]

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