The evolution of fruit color: phylogeny, abiotic factors and the role of mutualists

​果实颜色的演化:系统发育、非生物因素及共生者的作用

The adaptive significance of fruit color has been investigated for over a century. While color can fulfill various functions, the most commonly tested hypothesis is that it has evolved to increase fruit visual conspicuousness and thus promote detection and consumption by seed dispersing animals. However, fruit color is a complex trait which is subjected to various constraints and selection pressures. As a result, the effect of animal selection on fruit colour are often difficult to identify, and several studies have failed to detect it. Here, we employ an integrative approach to examine what drives variation in fruit color.

水果颜色的适应性研究已有一个多世纪的历史。虽然颜色可以完成多种功能，但最常见的假设是，它已经进化到增加水果的视觉显著性，从而促进传播种子的动物的发现和消费。然而，水果的颜色是一个复杂的性状，它受到各种各样的限制和选择压力。因此，动物对水果颜色的选择的影响往往很难识别，一些研究未能发现它。在这里，我们采用一种综合的方法来研究是什么导致了水果颜色的变化。

We quantified the colour of ripe fruit and mature leaves of 97 tropical plant species from three study sites in Madagascar and Uganda. We used phylogenetically controlled models to estimate the roles of phylogeny, abiotic factors, and dispersal mode on fruit color variation. Our results show that, independent of phylogeny and leaf coloration, mammal dispersed fruits are greener than bird dispersed fruits, while the latter are redder than the former. In addition, fruit color does not correlate with leaf colour in the visible spectrum, but fruit reflection in the ultraviolet area of the spectrum is strongly correlated with leaf reflectance, emphasizing the role of abiotic factors in determining fruit color. These results demonstrate that fruit color is affected by both animal sensory ecology and abiotic factors and highlight the importance of an integrative approach which controls for the relevant confounding factors.

我们对马达加斯加和乌干达三个研究地点的97种热带植物的成熟果实和成熟叶片的颜色进行了量化。我们使用系统遗传学控制的模型来估计系统发育、非生物因素和分散模式对果实颜色变化的作用。结果表明，在不受系统发育和叶色影响的情况下，哺乳动物果实比鸟类果实更绿，鸟类果实比哺乳动物果实更红。此外，在可见光谱中，果实颜色与叶片颜色无关，但光谱中紫外区域的果实反射与叶片反射率密切相关，强调了非生物因素在决定果实颜色中的作用。这些结果表明，水果的颜色受动物感官生态和非生物因素的影响，并强调了控制相关混杂因素的综合方法的重要性。

Understanding the origin and adaptive significance of fruit color has been a lively source of debate for over a century. While less varied than flower color globally, fruit color diversity is nonetheless extensive, spanning and surpassing the human capacity to detect it. Fruit color diversity has been attributed to phylogenetic constraints, environmental constraints, and protection from antagonists. Yet the oldest, best documented, and most contentious hypothesis for why fruit color is so diverse centres on its role in attracting seed dispersing mutualists. The disperser hypothesis posits that the colour of fleshy fruits evolved to maximise visual detection by specific animal mutualists to facilitate seed dispersal.

了解水果颜色的起源和适应的意义是一个多世纪以来争论的一个活跃的来源。虽然水果的颜色在全球范围内不如花的颜色那么多样化，但水果的颜色多样性是广泛的，跨越并超过了人类对其的探测能力。果实颜色的多样性是由于系统发育的限制、环境的限制以及对拮抗物的保护。然而，关于水果颜色为何如此多样化的最古老、记载最充分、争议最大的假说，集中在它在吸引相互分散的种子方面所起的作用上。散布者假说假设，肉质水果的颜色进化是为了让特定的动物互惠主义者能够最大限度地观察到，从而促进种子的散布。

The finding that fruit and leaf reflectance in only the UV part of the spectrum are correlated may indicate the importance of solar radiation in fruit colour, at least across certain parts of the spectrum. While solar radiation is required to maintain plant function, excess light absorption can be damaging, and even fatal, to plant tissues，

发现只有光谱的紫外部分的水果和叶子的反射率是相关的，这可能表明太阳辐射对水果颜色的重要性，至少在光谱的某些部分。虽然维持植物的功能需要太阳辐射，但过量的光吸收对植物组织是有害的，甚至是致命的，这可能导致使用植物色素作为光保护膜。

Absorption at certain spectra, particularly in the ultraviolet, can result in photoinhibition and photodamage – reduced photosynthetic efficiency and cell damage. Plants have mechanisms to detect and respond to variation in ambient light, and to attenuate harmful solar radiation via investment incompounds.Plant UV reflectance may also function to reduce water loss in plant parts. Experimentally, UV reflectance has been found to increase likelihood of ripening, and responsive to both solar radiation and edaphic factors in temperate, agricultural systems.

某些光谱的吸收，特别是在紫外线下的吸收，会导致光抑制和光损伤——降低光合效率和细胞损伤。植物具有探测和响应环境光变化的机制，并通过对化合物的投资来减弱有害的太阳辐射。植物的紫外反射率也可以减少植物部分的水分流失。实验发现，在温带农业系统中，紫外线反射率增加了成熟的可能性，并且对太阳辐射和土壤因子都有反应。

In conclusion, our results confirm that fruit colour is largely independent of phylogeny and that it is affected by both abiotic factors and interaction with seed-dispersing animals. They join several recent studies which demonstrated the malleability of fruits to frugivore sensory and feeding ecology. Yet they also highlight the importance of the multivariate approach which recognises that fruit color is shaped by multidirectional selection pressures, and that only by considering them in concert can the effect of each be isolated and understood.

综上所述，我们的研究结果证实，果实颜色在很大程度上与系统发育无关，并且受非生物因素和与种子分散动物相互作用的影响。他们加入了最近的几项研究，这些研究表明，水果具有可塑性，可以在感官和饲养生态方面产生果味。然而，他们也强调了多元方法的重要性，这种方法认识到水果的颜色是由多方位的选择压力形成的，只有把它们结合起来考虑，才能孤立和理解每种颜色的影响。