Cryptic variation between species and the basis of hybrid performance.

Cryptic variation between species and the basis of hybrid performance.
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DOI:
10.1371/journal.pbio.1000429
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发表时间:
2010-07-20
期刊:
影响因子:
9.8
通讯作者:
Coen E
Coen E
中科院分区:
生物学1区
文献类型:
--
作者:
Rosas U;Barton NH;Copsey L;Barbier de Reuille P;Coen E

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对基因表达自然变异及其表型效应的研究为物种杂交种活力和不育的起源提供了新的见解。密切相关的物种之间的杂交产生了两个截然不同的结果。结果之一是,物种杂交体可能不如其亲本,例如,繁殖力较差。另一个是F1 杂交种可能表现出优越的性能(杂种优势),例如活力增强。尽管已经提出了各种假设来解释杂交的这两个方面,但它们的生物学基础仍然知之甚少。为了进一步了解这个问题,我们分析了基因表达变异可能发挥的作用。我们采用了金鱼草的一个保守性状,即花的不对称性,并确定了密切相关的物种之间潜在的调控基因表达的差异程度。我们发现,由于顺式作用差异,所分析的两个基因(CYC 和 RAD)的表达在物种之间存在显着差异。通过使用一系列突变等位基因制作定量基因型-表型图,我们证明该物种处于基因表达-形态学空间的平台期,因此该变异没有可检测到的表型效应。然而,通过遗传杂交将基因型移出高原,可以揭示表型差异。如果基因组可以在基因表达空间的有效中性区域内自由进化,我们的结果就可以很容易地解释。这种漂移的后果对于单个基因座来说可以忽略不计,但是当考虑整个基因组的多个基因座时,我们表明这种变异可能对表型和适应性产生显着影响,从而导致显着的漂移负荷。通过考虑这些对各种基因表达-适应性景观的影响,我们得出的结论是,F1 杂种可能会在保守性状(例如基本生理学)方面表现出更高的性能,但在其他方面表现出较低的性能。因此,我们的研究提供了一种新的方法来解释杂交性能的各个方面如何通过基因活性的自然变异而产生。生物学中的一个主要难题是为什么物种之间的杂交表现出两种相反的特征。一方面,杂种通常比其亲本更有活力或生产力,这种现象称为杂种活力或杂种优势。另一方面,它们往往表现出活力和生育能力下降,这被称为混合自卑。人们已经提出了各种理论来解释混合性能的这两个方面,但我们仍然缺乏对这些相互冲突的特征如何产生的连贯解释。为了解决这个问题,我们研究了亲本物种之间基因表达变异可能发挥的作用。通过测量这种变异及其对表型的影响,我们表明特定基因的表达可能在进化过程中在特定范围内自由变化。虽然当单独考虑每个基因座时,这种变异可能几乎没有表型效应,但多个基因变异的集体效应可能变得非常显着。利用理论群体遗传学的论据,我们展示了这些效应如何导致杂交优势和劣势,为杂交性能的古老问题提供了新的见解。
Studies on natural variation in gene expression and its phenotypic effects provide fresh insights into the origins of vigour and sterility in species hybrids. Crosses between closely related species give two contrasting results. One result is that species hybrids may be inferior to their parents, for example, being less fertile. The other is that F1 hybrids may display superior performance (heterosis), for example with increased vigour. Although various hypotheses have been proposed to account for these two aspects of hybridisation, their biological basis is still poorly understood. To gain further insights into this issue, we analysed the role that variation in gene expression may play. We took a conserved trait, flower asymmetry in Antirrhinum, and determined the extent to which the underlying regulatory genes varied in expression among closely related species. We show that expression of both genes analysed, CYC and RAD, varies significantly between species because of cis-acting differences. By making a quantitative genotype-phenotype map, using a range of mutant alleles, we demonstrate that the species lie on a plateau in gene expression-morphology space, so that the variation has no detectable phenotypic effect. However, phenotypic differences can be revealed by shifting genotypes off the plateau through genetic crosses. Our results can be readily explained if genomes are free to evolve within an effectively neutral zone in gene expression space. The consequences of this drift will be negligible for individual loci, but when multiple loci across the genome are considered, we show that the variation may have significant effects on phenotype and fitness, causing a significant drift load. By considering these consequences for various gene-expression–fitness landscapes, we conclude that F1 hybrids might be expected to show increased performance with regard to conserved traits, such as basic physiology, but reduced performance with regard to others. Thus, our study provides a new way of explaining how various aspects of hybrid performance may arise through natural variation in gene activity. A major conundrum in biology is why hybrids between species display two opposing features. On the one hand, hybrids are often more vigorous or productive than their parents, a phenomenon called hybrid vigor or hybrid superiority. On the other hand they often show reduced vigour and fertility, known as hybrid inferiority. Various theories have been proposed to account for these two aspects of hybrid performance, yet we still lack a coherent account of how these conflicting characteristics arise. To address this issue, we looked at the role that variation in gene expression between parental species may play. By measuring this variation and its effect on phenotype, we show that expression for specific genes may be free to vary during evolution within particular bounds. Although such variation may have little phenotypic effect when each locus is considered individually, the collective effect of variation across multiple genes may become highly significant. Using arguments from theoretical population genetics we show how these effects might lead to both hybrid superiority and inferiority, providing fresh insights into the age-old problem of hybrid performance.
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