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Egg pigmentation probably has an early Archosaurian origin
Nature ( IF 50.5 ) Pub Date : 2019-06-01 , DOI: 10.1038/s41586-019-1282-4 Matthew D Shawkey 1 , Liliana D'Alba 1
Nature ( IF 50.5 ) Pub Date : 2019-06-01 , DOI: 10.1038/s41586-019-1282-4 Matthew D Shawkey 1 , Liliana D'Alba 1
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Colours have crucial roles in the lives of organisms, from camouflage to mate and pollinator attraction. Although the colours of animals known only from fossils were once thought to be unknowable, recent advances have enabled some to be reconstructed, with important implications for their (Palaeo) ecology and evolution1. A recent paper2 used Raman spectroscopy to show evidence of preservation of the two colour-producing pigments in avian eggs (biliverdin and protoporphyrin IX) in fossil dinosaur eggs. The authors used these data to infer the colours of these eggs and, based on their presence and absence in extinct and extant clades, to suggest that colourful eggs had a single evolutionary origin in the Eumaniraptora, or bird-like dinosaurs2. This is clearly an exciting finding, and the potential detection of these pigments could indeed enable considerable advances in our understanding of the evolution of egg pigmentation. However, the presence of these two pigments in white avian eggs and crocodile (non-eumaniraptoran) eggs draws their conclusions into question. The presence of biliverdin and/or protoporphyrin IX does not inevitably mean that an egg is coloured. Both pigments are widespread, and biliverdin can be found in (among many other places) the blood of fish3 and the yolk of frog eggs4. When found in eggshells, they can cause brown or blue–green coloration, but many white avian eggs (for example, of chickens (Gallus gallus)5, white storks (Ciconia ciconia), wood pigeons (Columba palumbus)6 and swifts (Apus apus)7) contain the pigments in low levels. Indeed, an extensive survey concluded that pigment-free white eggs are rare6. An egg containing these pigments could thus either be coloured or not, depending on concentration. Raman data on organic signals, as implemented2, can only be interpreted in relative terms, and thus give no information on absolute concentration that in turn would inform on coloration. Furthermore, none of the fossil eggs (with the possible exception of the previously reported Heyuannia8) shows any evidence of preserved colour. A recent study9 suggested that coloured eggs become brown during diagenesis, but did not examine the fate of white eggs. Without such data, it is not possible to infer with certainty that a fossil egg was coloured. Nevertheless, all eggs with any potential signal of preserved pigment were classified as fully coloured and/or colour patterned2. Apparent patterning of these pigments into maculation and spotting, as well as distribution in the shell cross-section reminiscent of those in modern bird eggs could be argued to further support the hypothesis that fossil eggs were coloured. However, these analyses were only performed on fossil eggs already classified as pigmented, making this argument circular. Fossil eggs classified as unpigmented, or white eggs with small amounts of pigment, lacking maculation patterns under the Raman surface-mapping analyses would obviously support the hypothesis that these eggs were coloured. But these critical negative controls were not done. The authors’ argument for this omission is that Raman imaging data would only show patterns of background noise. But the same may be true for eggs classified as pigmented. This possibility is particularly likely given that (1) the wavelengths chosen for Raman imaging analysis (1,160 cm−1 and 1,350 cm−1) are outside of the diagnostic Raman ‘fingerprint’ region, and (2) all ‘unpigmented’ fossil eggs show strong peaks at 1,160 cm−1, whereas most ‘pigmented’ eggs have valleys, rather than peaks, at 1,350 cm−1 (see Extended Data Fig. 1). Thus, these imaging data, although intriguing, provide no further support for colouring of fossil eggs. It could be argued that the low concentrations of pigments found in white eggs are unlikely to be preserved, but this needs to be tested directly and was not done in a related recent study9. Even if we do not definitively know that dinosaur eggs were coloured, it is still interesting and relevant that they may have been physiologically capable of depositing pigments in their eggs. However, the authors’ titular conclusion, that this capability had a single origin at the base of eumaniraptorans, is challenged both by the above and even more directly by the recent detection of protoporphyrin in white Siamese crocodile eggs10 (Fig. 1). Crocodiles are phylogenetically distant from eumaniraptorans, and a new maximum likelihood ancestral state reconstruction that includes them indicates a 67% probability of egg
中文翻译：
鸡蛋色素沉着可能有早期的始祖龙起源
颜色在生物体的生命中起着至关重要的作用，从伪装到配偶和传粉者的吸引力。尽管仅从化石中知道的动物的颜色曾经被认为是不可知的，但最近的进展已经使一些能够被重建，对它们的（古）生态和进化具有重要意义。最近的一篇论文 2 使用拉曼光谱显示了恐龙蛋化石中鸟类蛋（胆绿素和原卟啉 IX）中两种产生颜色的色素的保存证据。作者使用这些数据来推断这些蛋的颜色，并根据它们在已灭绝和现存进化枝中的存在和缺失，表明彩色蛋在真盗龙或类似鸟类的恐龙中具有单一的进化起源。这显然是一个令人兴奋的发现，这些色素的潜在检测确实可以使我们对鸡蛋色素沉着演变的理解取得相当大的进展。然而，这两种色素存在于白色鸟类蛋和鳄鱼（非真盗龙）蛋中，使他们的结论受到质疑。胆绿素和/或原卟啉 IX 的存在并不必然意味着鸡蛋是有颜色的。这两种色素都很普遍，胆绿素可以在（以及许多其他地方）鱼的血液 3 和蛙卵的蛋黄 4 中找到。当在蛋壳中发现时，它们会导致棕色或蓝绿色，但许多白色禽蛋（例如，鸡 (Gallus gallus)5、白鹳 (Ciconia ciconia)、木鸽 (Columba palumbus)6 和雨燕 (Apus apus)7) 含有少量色素。确实，一项广泛的调查得出结论，无色素的白鸡蛋很少见6。因此，含有这些色素的鸡蛋可以着色或不着色，具体取决于浓度。所实施的有机信号的拉曼数据只能以相对术语解释，因此无法提供有关绝对浓度的信息，而这些信息又会告知着色。此外，没有任何化石蛋（可能除了先前报道的河源虫 8 ）显示出任何保存颜色的证据。最近的一项研究 9 表明，有色鸡蛋在成岩过程中会变成棕色，但没有检查白色鸡蛋的命运。如果没有这些数据，就不可能肯定地推断出化石蛋是有颜色的。尽管如此，所有具有任何潜在色素保存信号的鸡蛋都被归类为完全着色和/或彩色图案2。这些色素的明显图案形成斑点和斑点，以及在壳横截面上的分布，让人想起现代鸟蛋中的那些，可以进一步支持化石蛋是有色的假设。然而，这些分析只对已经被归类为有色素的蛋化石进行，使这一论点成为循环。在拉曼表面映射分析下，被归类为无色素或含有少量色素的白蛋，缺乏斑纹图案的化石蛋显然支持这些蛋是有色的假设。但是这些关键的阴性对照没有完成。作者对这一遗漏的论点是拉曼成像数据只会显示背景噪声的模式。但对于被分类为有色的鸡蛋来说，情况可能也是如此。考虑到（1）为拉曼成像分析选择的波长（1,160 cm-1 和 1,350 cm-1）在诊断拉曼“指纹”区域之外，并且（2）所有“未着色”的化石蛋显示，这种可能性尤其可能在 1,160 cm-1 处有强烈的峰，而大多数“有色”卵在 1,350 cm-1 处有谷，而不是峰（参见扩展数据图 1）。因此，这些成像数据虽然很有趣，但并没有为化石蛋的着色提供进一步的支持。可以说，在白鸡蛋中发现的低浓度色素不太可能被保存，但这需要直接测试，并且在最近的一项相关研究中没有进行。即使我们不能确定恐龙蛋是有颜色的，但它们可能在生理上能够在它们的蛋中沉积色素仍然是有趣和相关的。然而，作者的名义结论是，这种能力在真盗龙的基础上具有单一起源，受到上述挑战，甚至更直接地受到最近在白色暹罗鳄鱼卵中检测到原卟啉的挑战（图 1）。鳄鱼在系统发育上与真盗龙相距甚远，包括它们在内的新的最大似然祖先状态重建表明产卵的概率为 67%
更新日期：2019-06-01
中文翻译：
鸡蛋色素沉着可能有早期的始祖龙起源
颜色在生物体的生命中起着至关重要的作用，从伪装到配偶和传粉者的吸引力。尽管仅从化石中知道的动物的颜色曾经被认为是不可知的，但最近的进展已经使一些能够被重建，对它们的（古）生态和进化具有重要意义。最近的一篇论文 2 使用拉曼光谱显示了恐龙蛋化石中鸟类蛋（胆绿素和原卟啉 IX）中两种产生颜色的色素的保存证据。作者使用这些数据来推断这些蛋的颜色，并根据它们在已灭绝和现存进化枝中的存在和缺失，表明彩色蛋在真盗龙或类似鸟类的恐龙中具有单一的进化起源。这显然是一个令人兴奋的发现，这些色素的潜在检测确实可以使我们对鸡蛋色素沉着演变的理解取得相当大的进展。然而，这两种色素存在于白色鸟类蛋和鳄鱼（非真盗龙）蛋中，使他们的结论受到质疑。胆绿素和/或原卟啉 IX 的存在并不必然意味着鸡蛋是有颜色的。这两种色素都很普遍，胆绿素可以在（以及许多其他地方）鱼的血液 3 和蛙卵的蛋黄 4 中找到。当在蛋壳中发现时，它们会导致棕色或蓝绿色，但许多白色禽蛋（例如，鸡 (Gallus gallus)5、白鹳 (Ciconia ciconia)、木鸽 (Columba palumbus)6 和雨燕 (Apus apus)7) 含有少量色素。确实，一项广泛的调查得出结论，无色素的白鸡蛋很少见6。因此，含有这些色素的鸡蛋可以着色或不着色，具体取决于浓度。所实施的有机信号的拉曼数据只能以相对术语解释，因此无法提供有关绝对浓度的信息，而这些信息又会告知着色。此外，没有任何化石蛋（可能除了先前报道的河源虫 8 ）显示出任何保存颜色的证据。最近的一项研究 9 表明，有色鸡蛋在成岩过程中会变成棕色，但没有检查白色鸡蛋的命运。如果没有这些数据，就不可能肯定地推断出化石蛋是有颜色的。尽管如此，所有具有任何潜在色素保存信号的鸡蛋都被归类为完全着色和/或彩色图案2。这些色素的明显图案形成斑点和斑点，以及在壳横截面上的分布，让人想起现代鸟蛋中的那些，可以进一步支持化石蛋是有色的假设。然而，这些分析只对已经被归类为有色素的蛋化石进行，使这一论点成为循环。在拉曼表面映射分析下，被归类为无色素或含有少量色素的白蛋，缺乏斑纹图案的化石蛋显然支持这些蛋是有色的假设。但是这些关键的阴性对照没有完成。作者对这一遗漏的论点是拉曼成像数据只会显示背景噪声的模式。但对于被分类为有色的鸡蛋来说，情况可能也是如此。考虑到（1）为拉曼成像分析选择的波长（1,160 cm-1 和 1,350 cm-1）在诊断拉曼“指纹”区域之外，并且（2）所有“未着色”的化石蛋显示，这种可能性尤其可能在 1,160 cm-1 处有强烈的峰，而大多数“有色”卵在 1,350 cm-1 处有谷，而不是峰（参见扩展数据图 1）。因此，这些成像数据虽然很有趣，但并没有为化石蛋的着色提供进一步的支持。可以说，在白鸡蛋中发现的低浓度色素不太可能被保存，但这需要直接测试，并且在最近的一项相关研究中没有进行。即使我们不能确定恐龙蛋是有颜色的，但它们可能在生理上能够在它们的蛋中沉积色素仍然是有趣和相关的。然而，作者的名义结论是，这种能力在真盗龙的基础上具有单一起源，受到上述挑战，甚至更直接地受到最近在白色暹罗鳄鱼卵中检测到原卟啉的挑战（图 1）。鳄鱼在系统发育上与真盗龙相距甚远，包括它们在内的新的最大似然祖先状态重建表明产卵的概率为 67%
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