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Review
. 2005 May 3;102 Suppl 1(Suppl 1):6535-42.
doi: 10.1073/pnas.0501847102. Epub 2005 Apr 25.

Chromosome speciation: humans, Drosophila, and mosquitoes

Francisco J Ayala  1 , Mario Coluzzi
Affiliations
Review

Chromosome speciation: humans, Drosophila, and mosquitoes

Francisco J Ayala et al. Proc Natl Acad Sci U S A. .

Abstract

Chromosome rearrangements (such as inversions, fusions, and fissions) may play significant roles in the speciation between parapatric (contiguous) or partly sympatric (geographically overlapping) populations. According to the "hybrid-dysfunction" model, speciation occurs because hybrids with heterozygous chromosome rearrangements produce dysfunctional gametes and thus have low reproductive fitness. Natural selection will, therefore, promote mutations that reduce the probability of intercrossing between populations carrying different rearrangements and thus promote their reproductive isolation. This model encounters a disabling difficulty: namely, how to account for the spread in a population of a chromosome rearrangement after it first arises as a mutation in a single individual. The "suppressed-recombination" model of speciation points out that chromosome rearrangements act as a genetic filter between populations. Mutations associated with the rearranged chromosomes cannot flow from one to another population, whereas genetic exchange will freely occur between colinear chromosomes. Mutations adaptive to local conditions will, therefore, accumulate differentially in the protected chromosome regions so that parapatric or partially sympatric populations will genetically differentiate, eventually evolving into different species. The speciation model of suppressed recombination has recently been tested by gene and DNA sequence comparisons between humans and chimpanzees, between Drosophila species, and between species related to Anopheles gambiae, the vector of malignant malaria in Africa.

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Figures

Fig. 1.
Fig. 1.
Two populations share a common boundary where hybridization occurs. Shown are two metacentric chromosomes that differ by an inversion (box) and incompatible alleles at two loci (*). Gene flow can readily occur along regions not linked to the inverted region (solid arrows) but is severely inhibited in regions linked to the inversion (dotted arrows). Natural selection favors the evolution of reproductive isolation between the populations by accumulation of incompatible alleles along the chromosome regions protected from recombination by the inversions. Figure was modified from ref. .
Fig. 2.
Fig. 2.
Geographic distribution of A. gambiae and six other closely related species. A. arabiensis, descended from a Pyretophorus species from the Arabian peninsula, is the likely ancestral species of the complex (see Fig. 3). Originally, A. arabiensis was zoophilic and exophilic, but it became anthropophilic and domestic by gradual adaptation to the human environment in Sudan and western Africa. A. quadriannulatus A and A. quadriannulatus B retain the original zoophily and exophily of their ancestral homonymous species, which also gave rise to A. bwambae and A. melas, and to A. gambiae, the most effective vector of malignant human malaria. A. gambiae and its strong anthropophily evolved <4000 B.P. with human invasion of the rain forest and introduction of slash-and-burn agriculture. In western Africa, A. gambiae is well represented in the Sahel region, extending up to 18° N, also the northern limit of A. arabiensis. In the Sudan, A. arabiensis, but not A. gambiae, is found along the river Nile upwards to the Egyptian border. Genetic data indicate that A. merus descends from A. gambiae and became adapted to breed in brackish, tide-dependent pools independently of A. melas.
Fig. 3.
Fig. 3.
Phylogeny of seven species and three incipient species related to A. gambiae. The likely ancestral species is A. arabiensis, which differs from A. quadriannulatus by three X-chromosome inversions and differs from A. gambiae by two additional X-chromosome inversions. Reproductive factors among these species are primarily located on the X chromosome. Several incipient species can be recognized that are related to A. arabiensis, A. melas, or A. gambiae. Three incipient species related to A. gambiae, labeled Savanna, Mopti, and Bamako, are shown.
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