Extensive introgression in a malaria vector species complex revealed by phylogenomics

Introduction The notion that species boundaries can be porous to introgression is increasingly accepted. Yet the broader role of introgression in evolution remains contentious and poorly documented, partly because of the challenges involved in accurately identifying introgression in the very groups where it is most likely to occur. Recently diverged species often have incomplete reproductive barriers and may hybridize where they overlap. However, because of retention and stochastic sorting of ancestral polymorphisms, inference of the correct species branching order is notoriously challenging for recent speciation events, especially those closely spaced in time. Without knowledge of species relationships, it is impossible to identify instances of introgression. Rationale Since the discovery that the single mosquito taxon described in 1902 as Anopheles gambiae was actually a complex of several closely related and morphologically indistinguishable sibling species, the correct species branching order has remained controversial and unresolved. This Afrotropical complex contains the world’s most important vectors of human malaria, owing to their close association with humans, as well as minor vectors and species that do not bite humans. On the basis of ecology and behavior, one might predict phylogenetic clustering of the three highly anthropophilic vector species. However, previous phylogenetic analyses of the complex based on a limited number of markers strongly disagree about relationships between the major vectors, potentially because of historical introgression between them. To investigate the history of the species complex, we used whole-genome reference assemblies, as well as dozens of resequenced individuals from the field. Results We observed a large amount of phylogenetic discordance between trees generated from the autosomes and X chromosome. The autosomes, which make up the majority of the genome, overwhelmingly supported the grouping of the three major vectors of malaria, An. gambiae, An. coluzzii, and An. arabiensis. In stark contrast, the X chromosome strongly supported the grouping of An. arabiensis with a species that plays no role in malaria transmission, An. quadriannulatus. Although the whole-genome consensus phylogeny unequivocally agrees with the autosomal topology, we found that the topology most often located on the X chromosome follows the historical species branching order, with pervasive introgression on the autosomes producing relationships that group the three highly anthropophilic species together. With knowledge of the correct species branching order, we are further able to uncover introgression between another species pair, as well as a complex history of balancing selection, introgression, and local adaptation of a large autosomal inversion that confers aridity tolerance. Conclusion We identify the correct species branching order of the An. gambiae species complex, resolving a contentious phylogeny. Notably, lineages leading to the principal vectors of human malaria were among the first in the complex to radiate and are not most closely related to each other. Pervasive autosomal introgression between these human malaria vectors, including nonsister vector species, suggests that traits enhancing vectorial capacity can be acquired not only through de novo mutation but also through a more rapid process of interspecific genetic exchange. Time-lapse photographs of an adult anopheline mosquito emerging from its pupal case. RELATED ITEMS IN ScienceD. E. Neafsey et al., Science 347, 1258522 (2015) Introgressive hybridization is now recognized as a widespread phenomenon, but its role in evolution remains contested. Here, we use newly available reference genome assemblies to investigate phylogenetic relationships and introgression in a medically important group of Afrotropical mosquito sibling species. We have identified the correct species branching order to resolve a contentious phylogeny and show that lineages leading to the principal vectors of human malaria were among the first to split. Pervasive autosomal introgression between these malaria vectors means that only a small fraction of the genome, mainly on the X chromosome, has not crossed species boundaries. Our results suggest that traits enhancing vectorial capacity may be gained through interspecific gene flow, including between nonsister species. Mosquito adaptability across genomes Virtually everyone has first-hand experience with mosquitoes. Few recognize the subtle biological distinctions among these bloodsucking flies that render some bites mere nuisances and others the initiation of a potentially life-threatening infection. By sequencing the genomes of several mosquitoes in depth, Neafsey et al. and Fontaine et al. reveal clues that explain the mystery of why only some species of one genus of mosquitoes are capable of transmitting human malaria (see the Perspective by Clark and Messer). Science, this issue 10.1126/science.1258524 and 10.1126/science.1258522; see also p. 27 Comparison of several genomes reveals the genetic history of mosquitoes’ ability to vector malaria among humans. [Also see Perspective by Clark and Messer]