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Understanding phylogenetic relationships within species complexes of disease vectors is crucial for identifying genomic changes associated with the evolution of epidemiologically important traits. However, the high degree of genetic similarity among sibling species confounds the ability to determine phylogenetic relationships using molecular markers. The goal of this study was to infer the ancestral–descendant relationships among malaria vectors and nonvectors of the  Anopheles gambiae  species complex by analyzing breakpoints of fixed chromosomal inversions in ingroup and several outgroup species. We identified genes at breakpoints of fixed overlapping chromosomal inversions 2Ro and 2Rp of  An. merus  using fluorescence  in situ  hybridization, a whole-genome mate-paired sequencing, and clone sequencing. We also mapped breakpoints of a chromosomal inversion 2La (common to  An. merus ,  An. gambiae , and  An. arabiensis ) in outgroup species using a bioinformatics approach. We demonstrated that the “standard” 2R+ p  arrangement and “inverted” 2Ro and 2La arrangements are present in outgroup species  Anopheles stephensi ,  Aedes aegypti , and  Culex quinquefasciatus . The data indicate that the ancestral species of the  An. gambiae  complex had the 2Ro, 2R+ p , and 2La chromosomal arrangements. The “inverted” 2Ro arrangement uniquely characterizes a malaria vector  An. merus  as the basal species in the complex. The rooted chromosomal phylogeny implies that  An. merus  acquired the 2Rp inversion and that its sister species  An. gambiae  acquired the 2R+ o  inversion from the ancestral species. The karyotype of nonvectors  An. quadriannulatus  A and B was derived from the karyotype of the major malaria vector  An. gambiae . We conclude that the ability to effectively transmit human malaria had originated repeatedly in the complex. Our findings also suggest that saltwater tolerance originated first in  An. merus  and then independently in  An. melas . The new chromosomal phylogeny will facilitate identifying the association of evolutionary genomic changes with epidemiologically important phenotypes.

A New Chromosomal Phylogeny Supports the Repeated Origin of Vectorial Capacity in Malaria Mosquitoes of the Anopheles gambiae Complex