Lineage divergence detected in the malaria vector Anopheles marajoara (Diptera: Culicidae) in Amazonian Brazil

Abstract

BackgroundCryptic species complexes are common among anophelines. Previous phylogenetic analysis based on the complete mtDNA COI gene sequences detected paraphyly in the Neotropical malaria vector Anopheles marajoara. The "Folmer region" detects a single taxon using a 3% divergence threshold.MethodsTo test the paraphyletic hypothesis and examine the utility of the Folmer region, genealogical trees based on a concatenated (white + 3' COI sequences) dataset and pairwise differentiation of COI fragments were examined. The population structure and demographic history were based on partial COI sequences for 294 individuals from 14 localities in Amazonian Brazil. 109 individuals from 12 localities were sequenced for the nDNA white gene, and 57 individuals from 11 localities were sequenced for the ribosomal DNA (rDNA) internal transcribed spacer 2 (ITS2).ResultsDistinct A. marajoara lineages were detected by combined genealogical analysis and were also supported among COI haplotypes using a median joining network and AMOVA, with time since divergence during the Pleistocene (<100,000 ya). COI sequences at the 3' end were more variable, demonstrating significant pairwise differentiation (3.82%) compared to the more moderate 2.92% detected by the Folmer region. Lineage 1 was present in all localities, whereas lineage 2 was restricted mainly to the west. Mismatch distributions for both lineages were bimodal, likely due to multiple colonization events and spatial expansion (~798 - 81,045 ya). There appears to be gene flow within, not between lineages, and a partial barrier was detected near Rio Jari in Amapá state, separating western and eastern populations. In contrast, both nDNA data sets (white gene sequences with or without the retention of the 4th intron, and ITS2 sequences and length) detected a single A. marajoara lineage.ConclusionsStrong support for combined data with significant differentiation detected in the COI and absent in the nDNA suggest that the divergence is recent, and detectable only by the faster evolving mtDNA. A within subgenus threshold of >2% may be more appropriate among sister taxa in cryptic anopheline complexes than the standard 3%. Differences in demographic history and climatic changes may have contributed to mtDNA lineage divergence in A. marajoara.

Mitochondrial DNA Detects a Complex Evolutionary History with Pleistocene Epoch Divergence for the Neotropical Malaria Vector Anopheles nuneztovari Sensu Lato

“…However, this finding was consistent with the data of Calado and others 18 and with divergence estimates of other sister-taxa in the Nyssorhynchus subgenus. 61 Additionally, populations of An. nuneztovari s.l.…”

“…nuneztovari s.l., as detected in a previous study in this species, 26 and in other anophelines. [61][62][63] The samples from the Amazon Basin tended to have higher genetic diversity, in particular nucleotide diversity, than those from Bolivia/ Colombia/Venezuela. These differences were congruent with those of previous mitochondrial and nuclear gene studies 22,[25][26][27][28]64 and can be indicative of cryptic species, or possibly differences in effective population size ( N e) or other events related to the history of these populations.…”

“…28 The sharing of haplotypes across great distances may be the result of isolation, followed by secondary contact in an area known for its complex geologic changes. 68 Pleistocene epoch divergence has been detected for a wide range of insect species, 56, 69 including disease vectors, 28,61,63 suggesting climatic changes as an important force driving the speciation in the Neotropical region. In the present study, the divergence time estimated among all clades and subclades supported diversification during the Pleistocene Epoch.…”

Isolation and characterization of 25 microsatellite DNA loci for Anopheles albitarsis sensu lato and inter-specific amplification in 5 congeneric species

“…Of these species, the following are considered as malaria vectors in Brazil: A. deaneorum in Rondônia (Klein et al, 1991), A. marajoara in São Paulo, and Pará and Amapá (Conn et al, 2002;McKeon et al, 2010) and A. janconnae in Roraima (Povoa, 2006). Biochemical and/or molecular differences, eating habits, and anthropophily reflect the heterogeneity and capacity of the A. albitarsis s.l.…”

Hybrid sterility in crosses between two Brazilian sibling species of the Anopheles albitarsis complex

“…Lynch-Arribálzaga is widely distributed from northern Guatemala to northern Argentina [6] and is a complex of cryptic species that includes some of the most important regional vectors in America [7][8][9]. The first indication of An.…”