Mosquito evolution, chromosomal differentiation, and introgression

This paragraph from Ayala and Coluzzi (2005) gives an admirable synopsis of the causes for the evolution of falciparum malaria-bearing mosquito Anopheles gambiae:

The origins of A. gambiae can be traced to the late Neolithic, <4000 B.P. A. gambiae exhibits the primitive chromosome arrangement 2R (used within the complex as the standard of reference), which is adapted to the African rain forest, where, nevertheless, A. gambiae can only breed in environments modified by human agriculture, given that the larvae are "eliophilic," requiring sunlight for breeding (21). Agriculture was introduced in Africa 8000 B.P., imported from Mesopotamia into the lower Nile valley, but the forest remained for a long time impenetrable, without any traces of agricultural activity up to 4000 years B.P. Extensive penetration of the forest began 3000 B.P., made possible by climate change and the temporary "savannization" of much of the central African rain forest, a process which began 2800 B.P. and lasted 5 centuries (41). When the forest belt regained its original range of distribution, 2300 B.P., it was invaded by Bantu agriculturalists who adopted "slash-and-burn" agricultural techniques. Increase in rainfall and the return of the forest were determinant factors for the spreading of the tze-tze fly (Glossina), vector of the lethal animal trypanosomiasis (Trypanosoma brucei), which decimated cattle, thus promoting the adaptation of A. quadriannulatus to humans, who became an easy host for the blood meal and, more importantly, caused the opening of the forest canopy. These conditions promoted strong selection for anthropophily and domesticity, which facilitated the evolution of A. gambiae (20, 41). There was a consequent increase in the rate of human infection by P. falciparum, which in turn led to strong selection for highly virulent strains, such as are the current forms of this parasite. Genetic evidence indicates that the expansion of malignant P. falciparum in Africa and throughout the world tropics occurred only within the last few thousand years (42-44).

It's quite a complicated series of events, initiated by the irresistable force of human population growth, but spurred at a particular moment by short-term climate change.

Additionally, despite the presence of fixed X chromosome inversions between the species (A. gambiae and A. arabiensis), there appears to have been introgression of some genes from one species into the other on the autosomes, which still have polymorphic inversions:

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. These results are consistent with the suppressed-recombination model because the X chromosomes of the two species are fixed for different inversions, where reproductive factors are located.
The shared nucleotide polymorphisms in the autosomal chromosomes may, however, be ancestral rather than originated by recent gene flow between the two species. An investigation of the ND5 locus of mitochondrial DNA shows that ancestral haplotypes persist in the two species, A. gambiae and A. arabiensis (49). 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).

This reference 48 is a paper by Besansky et al. (2003):

Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: Evidence from multilocus DNA sequence variation
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.

There's more in the Ayala and Coluzzi (2005) article, including a long section on the possible importance of chromosomal rearrangements in the divergence of chimpanzees and humans that merits some comment. The bottom line is that chromosomes that underwent reorganization during human evolution appear to have a higher rate of amino acid substitution and a higher rate of change of functional expression than chromosomes that remain aligned with their chimpanzee homologs. They discuss several reasons why this might be, but conclude that most likely the rearranged chromosomes just have a higher number of genes that have been positively selected.


Ayala FJ, Coluzzi M. 2005. Chromosome speciation: Humans, Drosophila, and mosquitoes. PNAS 102: 6535-6542. Full text

Besansky NJ et al. 2003. Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: Evidence from multilocus DNA sequence variation. PNAS 100: 10818-10823 Full text