A new species in the major malaria vector complex sheds light on reticulated species evolution

Abstract

Complexes of closely related species provide key insights into the rapid and independent evolution of adaptive traits. Here, we described and studied Anopheles fontenillei sp.n., a new species in the Anopheles gambiae complex that we recently discovered in the forested areas of Gabon, Central Africa. Our analysis placed the new taxon in the phylogenetic tree of the An. gambiae complex, revealing important introgression events with other members of the complex. Particularly, we detected recent introgression, with Anopheles gambiae and Anopheles coluzzii, of genes directly involved in vectorial capacity. Moreover, genome analysis of the new species allowed us to clarify the evolutionary history of the 3La inversion. Overall, An. fontenillei sp.n. analysis improved our understanding of the relationship between species within the An. gambiae complex, and provided insight into the evolution of vectorial capacity traits that are relevant for the successful control of malaria in Africa.

Figure 1

Overview of An. fontenillei bionomic characteristics. (A) Red points indicate the mosquito collection sites in the National Park of La Lopé where An. fontenillei specimens were captured. The bottom right corner shows a photograph of the breeding site where one larva of the new species was found. (B) Mean number (black dots) of An. fontenillei collected using human landing catch (human, red) vs. BG traps (trap, green) in the six sylvatic sites (A) Table S1). (C) Morphological features of An. fontenillei: dorsal view of the wing, maxillary palpus and hindleg with femur, tibia and tarsomeres. (D) Images of polytene chromosomes from ovarian nurse cells of An. fontenillei obtained with a contrast-phase microscope (specimen n. 23). Chromosomal arm karyotypes are indicated following the classical nomenclature. The paracentric inversions are designed by lines (red and blue) above the 3 R(b) and 3 L(a) arms, respectively.

Figure 2

Most common phylogenetic tree topology for the analysed X chromosome sequences of different An. gambiae complex species. 78 windows in the X chromosome show this tree topology with a weak disagreement in the most basal branch. Black numbers represent bootstrapping values, and red numbers the divergence (Ma, million years ago) estimated based on the pairwise distances of the ML phylogeny and assuming a substitution rate of 11 × 10⁻⁹ per site, per generation, and 10 generation per year.

Figure 3

Relationships of An. fontenillei with other species in the An. gambiae complex according to the phylogenetic trees in 50 kb non-overlapping windows along each chromosome arm. For each chromosomal arm, (A) refers to after speciation and (B) refers to before speciation of An. fontenillei with An. bwambae.

Figure 4

Species topology estimated from the X chromosome sequences compared with the topology of the 3La inversion. An. christyi was used as outgroup species. Green colour: possible introgression between An. arabiensis and the An. gambiae – An. coluzzii clade common ancestor. Purple colour: species that share the 3La inversion. Yellow colour: possible introgression event between An. quadriannulatus and An. merus.