Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation.

Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation.
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DOI:
10.1371/journal.pgen.1005141
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发表时间:
2015-04
期刊:
影响因子:
4.5
通讯作者:
Tripet F
Tripet F
中科院分区:
生物学2区
文献类型:
--
作者:
Aboagye-Antwi F;Alhafez N;Weedall GD;Brothwood J;Kandola S;Paton D;Fofana A;Olohan L;Betancourth MP;Ekechukwu NE;Baeshen R;Traorè SF;Diabate A;Tripet F

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虽然许多同域物种形成的理论模型提出,负责早期物种之间的交配的基因应该与基因组区域保护重组,有很少的数据来支持这一理论。冈比亚按蚊以其通过交配前生殖隔离维持的同域隐蔽物种和其假定的物种形成基因组岛而闻名,因此是研究与初期同域物种形成相关的基因组签名的理想模型系统。在这里,我们选择性地渐渗岛的分歧位于臂间区的X染色体的An。冈比亚有限公司它的姐妹分类群An。coluzzii通过5代回交,然后在渗入菌株内进行两代杂交,产生An.在X染色体岛上固定了M和S标记的coluzzii样重组菌株。然后,通过给予未使用的重组个体选择与其自身的岛类型匹配和不匹配的X-岛的配偶来测试重组菌株的交配偏好。我们表明,通过遗传分析的转移精子,重组女性一贯交配匹配岛型男性,从而关联的X-岛的分歧,交配基因。此外,全基因组测序证实,重组菌株之间的蛋白质编码差异仅限于实验交换的着丝粒周围区域。最后,靶基因组比较表明,这些独特的差异是保守的同域场人口,从而揭示候选物种形成基因。物种形成基因和分化的X-岛之间的密切联系的功能演示提供了前所未有的支持岛屿的物种形成模型的同域物种形成促进臂间重组抑制。 冈比亚按蚊是非洲最重要的疟疾传播媒介。该物种正在经历物种形成,并已确定了一些亚群,可以产生可行的杂交后代,但生殖隔离通过重复交配和生态适应。这种复杂的结构为研究物种形成所需的独特遗传和行为过程提供了理想的系统。冈比亚按蚊的亚种群在基因组中被称为物种形成岛的有限区域内存在遗传差异。理论研究预测,这些岛,其特征是有限的基因重排,可能会保护新兴物种之间的交配基因,是物种形成过程的基础。我们着手测试这一预测进行复杂的遗传杂交之间的姐妹物种按蚊coluzzii和冈比亚按蚊s.s.并产生重组菌株,其差异仅在于它们的X染色体物种形成岛。我们表明,通过行为研究,重组女性一贯交配匹配岛型男性,从而关联的X-岛的分歧,选择性交配基因。通过对重组菌株和自然群体的遗传密码进行测序,我们可以证实这些发现,并确定候选的选择性交配基因。这些研究结果表明,与物种形成相关的遗传和行为过程的分歧岛的重要作用。
Although many theoretical models of sympatric speciation propose that genes responsible for assortative mating amongst incipient species should be associated with genomic regions protected from recombination, there are few data to support this theory. The malaria mosquito, Anopheles gambiae, is known for its sympatric cryptic species maintained by pre-mating reproductive isolation and its putative genomic islands of speciation, and is therefore an ideal model system for studying the genomic signature associated with incipient sympatric speciation. Here we selectively introgressed the island of divergence located in the pericentric region of the X chromosome of An. gambiae s.s. into its sister taxon An. coluzzii through 5 generations of backcrossing followed by two generations of crosses within the introgressed strains that resulted in An. coluzzii-like recombinant strains fixed for the M and S marker in the X chromosome island. The mating preference of recombinant strains was then tested by giving virgin recombinant individuals a choice of mates with X-islands matching and non-matching their own island type. We show through genetic analyses of transferred sperm that recombinant females consistently mated with matching island-type males thereby associating assortative mating genes with the X-island of divergence. Furthermore, full-genome sequencing confirmed that protein-coding differences between recombinant strains were limited to the experimentally swapped pericentromeric region. Finally, targeted-genome comparisons showed that a number of these unique differences were conserved in sympatric field populations, thereby revealing candidate speciation genes. The functional demonstration of a close association between speciation genes and the X-island of differentiation lends unprecedented support to island-of-speciation models of sympatric speciation facilitated by pericentric recombination suppression. Anopheles gambiae is the most important vector of malaria in Africa. This species is undergoing speciation and a number of subpopulations have been identified which can produce viable hybrid offspring but are reproductively isolated through assortative mating and ecological adaptation. This complex structure provides an ideal system for studying the unique genetic and behavioural processes required for speciation. Anopheles gambiae’s subpopulations differ genetically in limited regions of their genomes called islands of speciation. Theoretical studies predict that these islands, characterized by restricted genetic rearrangements, may protect genes of assortative mating between emerging species, and are fundamental to the speciation process. We set out to test this prediction by performing complex genetic crosses between the sister species Anopheles coluzzii and Anopheles gambiae s.s. and creating recombinant strains differing only at their X-chromosome island of speciation. We show through behavioural studies that recombinant females consistently mated with matching island-type males thereby associating assortative mating genes with the X-island of divergence. By sequencing the genetic code of the recombinant strains and natural populations, we could confirm these findings and identify candidate assortative mating genes. These findings suggest an important role of divergence islands for the genetic and behavioural processes associated with speciation.
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