Semipermeable species boundaries betweenAnopheles gambiaeandAnopheles arabiensis: Evidence from multilocus DNA sequence variation

Abstract

Attempts to reconstruct the phylogenetic history of the Anopheles gambiae cryptic species complex have yielded strongly conflicting results. In particular, An. gambiae, the primary African malaria vector, is variously placed as a sister taxon to either Anopheles arabiensis or Anopheles merus. The recent divergence times for members of this complex complicate phylogenetic analysis, making it difficult to unambiguously implicate interspecific gene flow, versus retained ancestral polymorphism, as the source of conflict. Using sequences at four unlinked loci, which were determined from multiple specimens within each of five species in the complex, we found contrasting patterns of sequence divergence between the X chromosome and the autosomes. The isolation model of speciation assumes a lack of gene flow between species since their separation. This model could not be rejected for An. gambiae and An. arabiensis, although the data fit the model poorly. On the other hand, evidence from gene trees supports genetic introgression of chromosome 2 inversions between An. gambiae and An. arabiensis, and also points to more broad scale genetic exchange of autosomal sequences between this species pair. That such exchange has been relatively recent is suggested not only by the lack of fixed differences at three autosomal loci but also by the sharing of full haplotypes at two of the three loci, which is in contrast to several fixed differences and considerably deeper divergence on the X. The proposed acquisition by An. gambiae of sequences from the more arid-adapted An. arabiensis may have contributed to the spread and ecological dominance of this malaria vector.

DNA barcoding mosquitoes: advice for potential prospectors

“…Additionally mosquitoes often exist rather as closely related species complexes that, when studied intimately -as with the Anopheles gambiae complex in Africa -can be observed to be diverging at some parts of the genome under low recombination while other parts of the genome undergo gene flow (Besansky et al 2003;Reidenbach et al 2012). Do we split these into separate species or group them into one?…”

Chromosome speciation: Humans,Drosophila, and mosquitoes

“…An investigation of DNA sequence variation in four gene loci (one from each of chromosomes X and 2 and two from chromosome 3) sampled from multiple specimens shows considerable similarity of gene polymorphisms and even haplotypes between the two autosomal chromosomes of A. gambiae and A. arabiensis (48), which share polymorphic inversions. At the X chromosome locus, however, there are fixed nucleotide differences and greater overall nucleotide differentiation between A. gambiae and A. arabiensis.…”

“…Nevertheless, comparison of allopatric and sympatric populations suggests locale-specific unidirectional introgression from A. arabiensis into A. gambiae. Indeed, the acquisition by A. gambiae of alleles from the more arid-adapted A. arabiensis may have contributed to its spread and ecological dominance (48). A more definitive test of the suppressed-recombination model of chromosomal speciation would call for estimation of the K A ͞K S ratio in 20 or more genes distributed among the three chromosomes of these two species, as well as among the other five species and additional incipient species.…”

Speciation and phylogeography of the Southeast Asian Anopheles sundaicus complex

“…These results may suggest a possible introgression event (Tang et al, 1996), which was not revealed by mtDNA. Whereas the Malaysian Borneo clade remained isolated, a genetic admixture with unequal nuclear and mitochondrial gene flow during coexistence of the two lineages is suggested for the Continental and Indonesian clades (della Torre et al, 1997;Garcia-Paris et al, 2003;Gentile et al, 2002;Besansky et al, 2003).…”