Rapid speciation via the evolution of pre-mating isolation in the Iberá Seedeater
Rapid speciation via the evolution of pre-mating isolation in the Iberá Seedeater
复制标题
伊贝拉食籽虫通过交配前隔离的进化快速形成物种
作者：
Sheela P. Turbek;M. Browne;Adrián S. Di Giacomo;Cecilia Kopuchian;W. Hochachka;Cecilia Estalles;Darío A. Lijtmaer;P. Tubaro;L. F. Silveira;I. Lovette;R. Safran;Scott A. Taylor;L. Campagna
最近分化的物种的快速辐射为探索物种形成的驱动因素提供了一个极好的机会。卡普奇诺种鸟是南美洲的一种鸟类，其中包括一些在野外通常只能通过雄性羽毛和鸣叫来识别的物种。Turbek等人使用基因组和行为实验来确定这一群体中两个成员的潜在隔离因素，并发现，尽管完全是同域的，但雌性只与同种雄性交配，而且物种之间只有少数基因不同（参见Jarvis的观点）。因此，一个小小的基因重组和配偶选择的强化推动了这些重叠和非常相似的物种的分化。科学，本期p. eabc0256；另见第1312页。在阿根廷的一个国家公园里，雌性的选择推动了卷尾猴种鸟的分类交配和物种形成。生物在物种形成的早期阶段提供了一个机会来理解控制分类群之间生殖隔离的过程。生态或行为机制可以作为共同发生的物种在其分化开始时的杂交的强大障碍。在物种形成早期跟踪野生种群的交配决定可以提高我们对行为隔离如何促进分化的理解。南方卡普奇诺种籽动物（孢子目）是传播最快的鸟类之一，表现出非常低的生态和基因组差异。我们利用最近发现的一种capuchino物种ibera<e:1> Seedeater （S. iberaensis）来研究物种形成早期的预交配障碍的起源和重要性。通过结合基因组和行为分析，我们研究了(i)选型交配在维持物种边界中的作用，（ii）物种识别的表型特征，（iii）这些特征的基因组基础，以及（iv）这些基因组变异的起源。结果2001年首次发现伊比利亚孢子虫，在阿根廷北部伊比利亚<e:1>湿地的主要繁殖地与hypoxantha共生。在两个繁殖季节，我们找到了这两个物种的巢穴并收集了基因组样本。我们发现极低的全基因组分化，除了三个狭窄的区域位于不同的染色体。这些区域包含12个基因，其中3个与羽毛颜色有关（TYRP1， OCA2和HERC2）。在鸟类的视觉光谱中，低xantha孢子虫和iberaensis的雄性在颜色和鸣声上不同，但雌性在颜色上是无法区分的。因此，我们使用基因组数据来量化选型交配。每只雌性的物种特异性基因型总是与其配偶的基因型相匹配，尽管这两个物种拥有邻近的繁殖区域，同步繁殖，并在同一片草地上觅食，但仍表现出强烈的选择性交配。我们通过野外回放实验，测试了不同羽毛图案和鸣声在物种识别和交配前隔离中的重要性。我们选择了同种和异种鸣声和羽毛组合的领地雄性，并评估了它们的攻击行为反应。每个物种对同种的鸣声和羽毛的反应都最激烈，这证实了这两种特征都是用来识别性竞争对手的。最后，我们通过研究更广泛的卷尾猴辐射的基因组分化，研究了新的伊比利亚S.羽毛表型的起源。尽管在分化程度较高的地区，多个物种与伊比利亚卷尾猴共享变异，但这些变异在不同地区的特定组合将伊比利亚卷尾猴与所有其他卷尾猴区分开来。结论本研究表明，基于羽毛颜色和鸣声的选择性配偶选择是促进这些共同发生的卷尾猴物种之间分化的主要机制。尽管早期伊比利亚葡萄种的最终命运仍然不确定，但我们的研究结果说明了谱系是如何形成的，并迅速从共生物种中分离出来。我们的研究结果进一步表明，现有遗传变异的重组可以产生新的表型，然后通过性选择作为目标。基于这些特征的分类交配可能在物种形成早期维持物种边界，而随后的生殖障碍积累。新的交配信号限制了共存鸟类之间的基因流动。伊比利亚孢子菌于2001年首次被发现，其繁殖范围完全包含在S. hypoxantha的范围内。尽管极低的基因组分化，这两个物种交配选型。遗传分化集中在已知参与羽毛颜色的基因附近。野外实验表明，鸣声和羽毛都是用来识别性竞争对手的。行为隔离可以催化物种形成，并允许共同发生的生物体之间缓慢积累额外的生殖障碍。我们通过研究两种鸟类（Sporophila hypoxantha和最近发现的S. iberaensis）之间的交配前隔离的基因组和行为基础来说明这一过程是如何发生的，这两种鸟类属于南部卡普奇诺（capuchino）种子捕食者，这是一种最近的快速辐射，其特征是雄性羽毛颜色和鸣叫的变化。尽管这两个物种共存时没有明显的生态障碍，但我们记录了通过鸣叫和羽毛特征来识别物种的行为，以及与雄性羽毛模式相关的基因组区域相关的强分类交配。羽毛的分化可能起源于原有遗传变异的重组，这表明新的性信号是如何迅速产生并维持物种界限的。
Choosy females drive isolation Rapid radiations of recently diverged species represent an excellent opportunity for exploring drivers of speciation. The capuchino seedeaters, a group of South American birds, include a number of species that, in the field, are often discernable only through male plumage and song. Turbek et al. used genomes and behavioral experiments to identify potential isolating factors in two members of this group and found that, though entirely sympatric, females mated only with conspecific males and that only a few genes differed between the species (see the Perspective by Jarvis). Thus, a small reshuffling of genes and reinforcement through mate choice has driven divergence in these overlapping and very similar species. Science, this issue p. eabc0256; see also p. 1312 Females’ choices have driven assortative mating and speciation in capuchino seedeater birds in a national park in Argentina. INTRODUCTION Organisms in the early stages of speciation provide an opportunity to understand the processes that govern reproductive isolation between taxa. Ecological or behavioral mechanisms can serve as powerful barriers to the interbreeding of co-occurring species at the onset of their divergence. Tracking mating decisions within wild populations early in speciation can improve our understanding of how behavioral isolation promotes divergence. RATIONALE The southern capuchino seedeaters (Sporophila) are one of the most rapid avian radiations, showing remarkably low ecological and genomic divergence. We took advantage of the recent discovery of a capuchino species, the Iberá Seedeater (S. iberaensis), to study the origin and importance of pre-mating barriers early in speciation. By combining genomic and behavioral analyses, we examined (i) the role of assortative mating in the maintenance of species boundaries, (ii) the phenotypic traits underlying species recognition, (iii) the genomic basis of such traits, and (iv) the origin of these genomic variants. RESULTS Sporophila iberaensis was first observed in 2001 and co-occurs with S. hypoxantha throughout its main breeding location in the northern portion of the Iberá wetlands of Argentina. Across two breeding seasons, we located nests and collected genomic samples from both species. We found extremely low genome-wide differentiation, with the exception of three narrow regions located on different chromosomes. These regions contained 12 genes, three of which are involved in plumage coloration (TYRP1, OCA2, and HERC2). Sporophila hypoxantha and S. iberaensis males differ in coloration and song, but females are indistinguishable in coloration across the avian visual spectrum. We therefore used genomic data to quantify assortative mating. Each female’s species-specific genotype always matched the genotype of her mate, demonstrating strong assortative mating despite these two species holding neighboring breeding territories, breeding synchronously, and foraging together on the same grasses. We tested the importance of divergent plumage patterning and song in species recognition and pre-mating isolation through playback experiments in the field. We presented territorial males with combinations of conspecific and heterospecific song and plumage, and assessed their aggressive behavioral responses. Each species responded most aggressively to conspecific song and plumage, confirming that both traits are used to recognize sexual competitors. Finally, we investigated the origin of the novel S. iberaensis plumage phenotype by examining genomic differentiation across the broader capuchino radiation. Although multiple species shared variants with S. iberaensis in the areas of elevated differentiation, the specific combination of these variants across the divergent regions distinguished S. iberaensis from all other capuchinos. CONCLUSION Our findings point to pre-mating isolation through assortative mate choice, based on both plumage coloration and song, as a primary mechanism promoting divergence between these co-occurring capuchino species. Although the ultimate fate of the incipient S. iberaensis species remains uncertain, our findings illustrate how lineages can form and quickly become reproductively isolated from co-occurring, syntopic species. Our results further suggest that the reshuffling of existing genetic variation can generate novel phenotypes that are then targeted by sexual selection. Assortative mating based on these traits may maintain species boundaries early in speciation while subsequent reproductive barriers accumulate. Novel mating signals restrict gene flow between co-occurring bird species. Sporophila iberaensis was first observed in 2001 and has a breeding range contained entirely within that of S. hypoxantha. Despite extremely low genomic differentiation, both species mate assortatively. Genetic differentiation is concentrated near genes known to be involved in plumage coloration. Field experiments show that both song and plumage are used to recognize sexual competitors. Behavioral isolation can catalyze speciation and permit the slow accumulation of additional reproductive barriers between co-occurring organisms. We illustrate how this process occurs by examining the genomic and behavioral bases of pre-mating isolation between two bird species (Sporophila hypoxantha and the recently discovered S. iberaensis) that belong to the southern capuchino seedeaters, a recent, rapid radiation characterized by variation in male plumage coloration and song. Although these two species co-occur without obvious ecological barriers to reproduction, we document behaviors indicating species recognition by song and plumage traits and strong assortative mating associated with genomic regions underlying male plumage patterning. Plumage differentiation likely originated through the reassembly of standing genetic variation, indicating how novel sexual signals may quickly arise and maintain species boundaries.
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