Anthropogenic Habitat Disturbance and Ecological Divergence between Incipient Species of the Malaria Mosquito Anopheles gambiae

Abstract

BackgroundAnthropogenic habitat disturbance is a prime cause in the current trend of the Earth’s reduction in biodiversity. Here we show that the human footprint on the Central African rainforest, which is resulting in deforestation and growth of densely populated urban agglomerates, is associated to ecological divergence and cryptic speciation leading to adaptive radiation within the major malaria mosquito Anopheles gambiae.Methodology/Principal FindingsIn southern Cameroon, the frequency of two molecular forms–M and S–among which reproductive isolation is strong but still incomplete, was correlated to an index of urbanisation extracted from remotely sensed data, expressed as the proportion of built-up surface in each sampling unit. The two forms markedly segregated along an urbanisation gradient forming a bimodal cline of ∼6-km width: the S form was exclusive to the rural habitat, whereas only the M form was present in the core of densely urbanised settings, co-occurring at times in the same polluted larval habitats of the southern house mosquito Culex quinquefasciatus–a species association that was not historically recorded before.Conclusions/SignificanceOur results indicate that when humans create novel habitats and ecological heterogeneities, they can provide evolutionary opportunities for rapid adaptive niche shifts associated with lineage divergence, whose consequences upon malaria transmission might be significant.

Pollutants and insecticides drive local adaptation in African malaria mosquitoes

“…Finally, due to the extreme association between the most effective vectors of the An. gambiae complex and human habitats, a long-standing hypothesis has suggested that human-driven selection is the main modulator of ecological divergence between and within species (Coluzzi et al 1979(Coluzzi et al , 2002Kamdem et al 2012;Caputo et al 2014). Consistent with this hypothesis, we have found that urban and suburban mosquitoes are genetically differentiated from rural populations and exhibit strong signatures of recent selection at loci containing xenobiotic resistance genes.…”

“…3D-F). All populations described as "urban" were collected from the most urbanized areas of the city, which are characterized by a high frequency of built environments as described in Kamdem et al (2012).…”

“…coluzzii is driven by human-induced changes (Touré et al 1998;Wondji et al 2005;Slotman et al 2007;Pinto et al 2013;Caputo et al 2014). This hypothesis has been formulated based on ecological observations and population structure, but the genetic underpinnings still need to be clearly assessed by examining patterns of variation across the genome (Coluzzi et al 2002;Kamdem et al 2012;Caputo et al 2014).…”

Adaptive deletion in resistance gene duplications in the malaria vector Anopheles gambiae

“…gambiae s.s . prefers wetter areas, with small and ephemeral water bodies (Lehmann, Diabate, & Diabaté, 2008); species preferences seem different in forests of Central Africa (Kamdem et al., 2012). Dabiré et al.…”

What are species and why does it matter? Anopheline taxonomy and the transmission of malaria

“…coluzzii and An. gambiae, show a partial but marked ecological differentiation as described above, with M predominant in more urbanised, more polluted environments with longer-lasting, more predator-infested breeding habitats; whereas S predominates in more rural settings (Kamdem et al, 2012).…”