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.
Highlights
Environmental change is a driving force in speciation and the genesis of evolutionary novelty, prompting adaptive variation to emerge by means of natural selection [1]
In what follows we report that anthropogenic changes of the central African rainforest are associated to ecological divergence between M and S
Ecological Divergence of the Molecular Forms To test the hypothesis that forest populations of the molecular forms of An. gambiae segregate along anthropogenic environmental gradients, we surveyed a 50650 km area around the capital city of Cameroon, Yaounde (Fig. 1A), a region that was previously identified to be suitable to both M and S [29]
Summary
Environmental change is a driving force in speciation and the genesis of evolutionary novelty, prompting adaptive variation to emerge by means of natural selection [1]. Anthropogenic modifications of the environment can lead to ecological divergence and foster the rapid evolution of reproductive isolation between ecotypes [9]. This process is difficult to document in nature unless it is caught in action [10]. We have used ongoing cryptic speciation in forest populations of the most important afro-tropical malaria mosquito Anopheles gambiae sensu stricto to demonstrate that recent landscape transformations in the African equatorial rainforest, due to the growth of densely populated urban areas, are at the heart of adaptive ecological divergence of two incipient sibling species within this taxon. 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
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