Abstract

The major drivers of the extensive biodiversity of the Neotropics are proposed to be geological and tectonic events together with Pliocene and Pleistocene environmental and climatic change. Geographical barriers represented by the rivers Amazonas/Solimões, the Andes and the coastal mountain ranges in eastern Brazil have been hypothesized to lead to diversification within the primary malaria vector, Anopheles (Nyssorhynchus) darlingi Root, which primarily inhabits rainforest. To test this biogeographical hypothesis, we analyzed 786 single nucleotide polymorphisms (SNPs) in 12 populations of An. darlingi from across the complex Brazilian landscape. Both model-based (STRUCTURE) and non-model-based (Principal Components and Discriminant Analysis) analysis of population structure detected three major genetic clusters that correspond with newly described Neotropical biogeographical regions: 1) Atlantic Forest province (= southeast population); 2) Parana Forest province (= West Atlantic forest population, with one Chacoan population - SP); and 3) Brazilian dominion population (= Amazonian population with one Chacoan population - TO). Significant levels of pairwise genetic divergences were found among the three clusters, allele sharing among clusters was negligible, and geographical distance did not contribute to differentiation. We infer that the Atlantic forest coastal mountain range limited dispersal between the Atlantic Forest province and the Parana Forest province populations, and that the large, diagonal open vegetation region of the Chacoan dominion dramatically reduced dispersal between the Parana and Brazilian dominion populations. We hypothesize that the three genetic clusters may represent three putative species.

Highlights

  • Anopheles (Nyssorhynchus) darlingi Root is broadly distributed in Central and South America, extending from southeastern Mexico to northern Argentina and from east of the Andes to the Atlantic coast [1]

  • Anopheles darlingi was described by Root [4] based on morphological characters of the egg, fourth-instar larva, pupa, male and female collected in Caxiribú in the vicinity of Porto das Caixas, Rio de Janeiro state, Brazil

  • We propose to: 1) assess the level of structure among populations of An. darlingi throughout Brazil; 2) address how genetic diversity is distributed between and within the major forest domains of Amazonia and Atlantic Forest compared with Cerrado; 3) examine whether divergence among population subgroups from the Atlantic coast and central Amazonia, southern and northeast Brazil [13], are consistent with the early morphological division proposed between the variant An. paulistensis and An. darlingi; 4) address the hypothesis that the Amazonian population represents an unknown putative species; and 5) discuss patterns of structure in the context of Neotropical biogeographical regionalization [26]

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Summary

Introduction

Anopheles (Nyssorhynchus) darlingi Root is broadly distributed in Central and South America, extending from southeastern Mexico to northern Argentina and from east of the Andes to the Atlantic coast [1]. This species is the most aggressive and effective Neotropical malaria vector, primarily in the Amazon/Solimões River basin. Polymorphisms were observed in the banding pattern of the X and all four autosome arms of the salivary gland polytene chromosome of representatives of An. darlingi populations from three northern localities in the Amazon forest and one southern locality in the domain of Cerrado, inland São Paulo state, and considered to be linked with distinct vectorial capacity [7]. An. darlingi has been considered to be a monotypic species based on other data sets [15, 16]

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