Chromosomal inversions and ecotypic differentiation in Anopheles gambiae: the perspective from whole‐genome sequencing

Abstract

The molecular mechanisms and genetic architecture that facilitate adaptive radiation of lineages remain elusive. Polymorphic chromosomal inversions, due to their recombination-reducing effect, are proposed instruments of ecotypic differentiation. Here we study an ecologically diversifying lineage of An. gambiae, known as the Bamako chromosomal form based on its unique complement of three chromosomal inversions, to explore the impact of these inversions on ecotypic differentiation. We used pooled and individual genome sequencing of Bamako, typical (non-Bamako) An. gambiae, and the sister species An. coluzzii to investigate evolutionary relationships and genome-wide patterns of nucleotide diversity and differentiation among lineages. Despite extensive shared polymorphism and limited differentiation from the other taxa, Bamako clusters apart from the other taxa, and forms a maximally supported clade in neighbor-joining trees based on whole genome data (including inversions) or solely on collinear regions. Nevertheless, FST outlier analysis reveals that the majority of differentiated regions between Bamako and typical An. gambiae are located inside chromosomal inversions, consistent with their role in the ecological isolation of Bamako. Exceptionally differentiated genomic regions were enriched for genes implicated in nervous system development and signaling. Candidate genes associated with a selective sweep unique to Bamako contain substitutions not observed in sympatric samples of the other taxa, and several insecticide resistance gene alleles shared between Bamako and other taxa segregate at sharply different frequencies in these samples. Bamako represents a useful window into the initial stages of ecological and genomic differentiation from sympatric populations in this important group of malaria vectors.

No evidence for maintenance of a sympatricHeliconiusspecies barrier by chromosomal inversions

“…2015; Love et al. 2016), and an inversion enabling the spread of an adaptive cassette between species (Kirkpatrick and Barrett 2015) might produce a signal of elevated f d . However, we see very little evidence for deviations in these statistics within the handful of candidate inversions compared to the surrounding regions, with only one H. cydno inversion (Fig.…”

“…S11-S17) to look for evidence of variation in gene flow at the inversion relative to surrounding regions. An inversion acting as a species barrier typically produces a signal of elevated F ST and reduced admixture (here estimated using f d ; Aulard et al 2002;Deng et al 2008;Huynh et al 2011;Nachman and Payseur 2012;Fontaine et al 2015;Love et al 2016), and an inversion enabling the spread of an adaptive cassette between species (Kirkpatrick and Barrett 2015) might produce a signal of elevated f d . However, we see very little evidence for deviations in these statistics within the handful of candidate inversions compared to the surrounding regions, with only one H. cydno inversion (Fig.…”

Patterns of divergence across the geographic and genomic landscape of a butterfly hybrid zone associated with a climatic gradient

“…However, there are a number of relatively large differentiated regions that may be the result of suppressed recombination, illustrated by the introgression of what appear to be large genomic blocks (Figure c; ). The importance and potential of inversions in facilitating divergence during speciation has been well documented in a number of systems (Hoffmann & Rieseberg, ; Kirkpatrick & Barton, ; Love et al., ; Noor et al., ; Trickett & Butlin, ); however, their role in facilitating divergence in this system remains unknown. A recombination and linkage map for P. glaucus would help in identifying possible inversions and more generally the role recombination is playing in producing variable patterns of differentiation in this system.…”

“…S8). The importance and potential of inversions in facilitating divergence during speciation has been well documented in a number of systems (Hoffmann & Rieseberg, 2008;Kirkpatrick & Barton, 2006;Love et al, 2016;Noor et al, 2001;Trickett & Butlin, 1994); however, their role in facilitating divergence…”

The impact of biological invasion and genomic local adaptation on the geographical distribution of Aedes aegypti in Panama

“…The presence of climate adapted Ae. aegypti somewhat mirrors the finding that climate variables, most notably precipitation and temperature associated with altitudinal and latitudinal clines, are able to drive population differentiation in both Anopheles mosquitoes and Drosophila flies (35)(36)(37)(38). In the former, the Anopheles gambiae species complex is hypothesised to have radiated through ecological speciation driven by adaptation to aridity and in response to larval habitat competition.…”