Extensive introgression in a malaria vector species complex revealed by phylogenomics
Authors: Fontaine Michael C. , Pease James B. , Steele Aaron , Waterhouse Robert M. , Neafsey Daniel E. , Sharakhov Igor V. , Jiang Xiaofang , Hall Andrew B. , Catteruccia Flaminia , Kakani Evdoxia , Mitchell Sara N. , Wu Yi-Chieh , Smith Hilary A. , Love R. Rebecca , Lawniczak Mara K. , Slotman Michel A. , Emrich Scott J. , Hahn Matthew W. , Besansky Nora J. 
Published: November 2014

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.

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