Simard Frédéric, Ayala Diego, Kamdem Guy Colince, Pombi Marco, Etouna Joachim, Ose Kenji, Fotsing Jean-Marie, Fontenille Didier, Besansky Nora J, Costantini Carlo
Laboratoire de Lutte contre les Insectes Nuisibles, Institut de Recherche pour le Développement, UR016, 911 Av. Agropolis, Cedex 5, Montpellier, France.
BMC Ecol. 2009 May 21;9:17. doi: 10.1186/1472-6785-9-17.
Speciation among members of the Anopheles gambiae complex is thought to be promoted by disruptive selection and ecological divergence acting on sets of adaptation genes protected from recombination by polymorphic paracentric chromosomal inversions. However, shared chromosomal polymorphisms between the M and S molecular forms of An. gambiae and insufficient information about their relationship with ecological divergence challenge this view. We used Geographic Information Systems, Ecological Niche Factor Analysis, and Bayesian multilocus genetic clustering to explore the nature and extent of ecological and chromosomal differentiation of M and S across all the biogeographic domains of Cameroon in Central Africa, in order to understand the role of chromosomal arrangements in ecological specialisation within and among molecular forms.
Species distribution modelling with presence-only data revealed differences in the ecological niche of both molecular forms and the sibling species, An. arabiensis. The fundamental environmental envelope of the two molecular forms, however, overlapped to a large extent in the rainforest, where they occurred in sympatry. The S form had the greatest niche breadth of all three taxa, whereas An. arabiensis and the M form had the smallest niche overlap. Correspondence analysis of M and S karyotypes confirmed that molecular forms shared similar combinations of chromosomal inversion arrangements in response to the eco-climatic gradient defining the main biogeographic domains occurring across Cameroon. Savanna karyotypes of M and S, however, segregated along the smaller-scale environmental gradient defined by the second ordination axis. Population structure analysis identified three chromosomal clusters, each containing a mixture of M and S specimens. In both M and S, alternative karyotypes were segregating in contrasted environments, in agreement with a strong ecological adaptive value of chromosomal inversions.
Our data suggest that inversions on the second chromosome of An. gambiae are not causal to the evolution of reproductive isolation between the M and S forms. Rather, they are involved in ecological specialization to a similar extent in both genetic backgrounds, and most probably predated lineage splitting between molecular forms. However, because chromosome-2 inversions promote ecological divergence, resulting in spatial and/or temporal isolation between ecotypes, they might favour mutations in other ecologically significant genes to accumulate in unlinked chromosomal regions. When such mutations occur in portions of the genome where recombination is suppressed, such as the pericentromeric regions known as speciation islands in An. gambiae, they would contribute further to the development of reproductive isolation.
冈比亚按蚊复合体成员之间的物种形成被认为是由干扰选择和生态分化促进的，这些作用于通过多态性臂内染色体倒位而免受重组影响的一组适应基因。然而，冈比亚按蚊M和S分子型之间共享的染色体多态性以及它们与生态分化关系的信息不足，对这一观点提出了挑战。我们使用地理信息系统、生态位因子分析和贝叶斯多位点基因聚类，来探究在非洲中部喀麦隆所有生物地理区域中M和S的生态和染色体分化的性质及程度，以便了解染色体排列在分子型内部和之间的生态特化中的作用。
仅利用存在数据进行的物种分布建模揭示了两种分子型以及近缘种阿拉伯按蚊生态位的差异。然而，这两种分子型的基本环境包络在雨林中有很大程度的重叠，它们在那里同域分布。S型在所有三个分类单元中生态位宽度最大；而阿拉伯按蚊和M型的生态位重叠最小。对M和S核型的对应分析证实，分子型在响应界定喀麦隆主要生物地理区域的生态气候梯度时，共享相似的染色体倒位排列组合。然而，M和S的稀树草原核型沿着由第二排序轴定义的较小尺度环境梯度分离。种群结构分析确定了三个染色体簇，每个簇都包含M和S样本的混合。在M和S中，替代核型在不同环境中分离，这与染色体倒位具有很强的生态适应价值一致。
我们的数据表明，冈比亚按蚊第二条染色体上的倒位并非M和S型之间生殖隔离进化的原因。相反，它们在两种遗传背景中参与生态特化的程度相似，并且很可能早于分子型之间的谱系分裂。然而，由于2号染色体倒位促进生态分化，导致生态型之间的空间和/或时间隔离，它们可能有利于其他具有生态意义的基因中的突变在不连锁的染色体区域积累。当这种突变发生在基因组中重组受到抑制的部分，比如冈比亚按蚊中被称为物种形成岛的着丝粒周围区域时，它们将进一步促进生殖隔离的发展。
