Biochemical plasticity and the evolution of diet-breadth in toxic insects

寄主植物取食的进化是理解昆虫进化的关键，特别是种群对气候变化的反应。例如，对气候变暖做出良好反应的英国蝴蝶物种通常也会扩大或改变它们对寄主植物的利用模式，而那些受到影响的蝴蝶物种通常有一个狭窄的寄主植物范围。在这里，我们将探讨蝴蝶如何改变它们的生化反应，以允许利用不同的寄主植物。这是表型可塑性的一种形式，在不同的环境条件下，单一基因型可以产生不同的表型。可塑性是一种重要的适应性，它可以使生物体在多变和异质的环境中生存，并促进长期的分化和多样化。以植物为食的昆虫必须处理有毒的植物化学物质，但在某些情况下，这些毒素也可以为昆虫提供防御化学物质的重要来源。热带蝴蝶可以从西番莲宿主那里获得产氰毒素，也可以合成自己的化合物。我们已经证明这些蝴蝶可以根据寄主的化学成分在这两种策略之间切换。当幼虫的饮食缺乏可以隔离的毒素时，海螺会通过增加自身防御的生物合成来做出反应。这允许使用更广泛的西番莲物种，同时保持它们的化学防御。我们可以很容易地区分来自寄主植物的毒素和蝴蝶产生的毒素，使其成为一种容易量化的表型可塑性形式。然而，这种可塑性的遗传和生化基础及其对生态位分配的生态重要性尚不清楚。我们将首先解决生态环境问题，使用目标代谢组学在巴西和巴拿马具有良好特征的寄主植物使用地点跟踪不同季节的黑头猴的化学成分。接下来，我们将探讨不同策略之间的适应度权衡，解决在塑料物种Heliconius erato中切换策略的原因。我们将比较在不同饮食中长大的个体的生长速度和其他生活史特征。我们还将比较衍生的专门物种的隔离效率，该物种仅从特定的寄主植物中获取毒素。“可塑性第一”假说预测了衍生谱系中效率的提高。防御性化合物变异的另一个主要轴是它们对捕食的影响，我们将测量宿主植物衍生和合成毒素的毒性和厌恶性。第三，我们将探索可塑性是如何受基因控制的，测试可塑性分子控制的两种假设。利用转录组学，我们将估计基因表达对幼虫饮食（存在和不存在宿主植物来源的毒素）的响应变化，并测试可塑性是否在蛋白质调节水平上受到控制。最后，我们将探索整个Heliconiines的氰生物合成的进化史，使用跨全基因组序列的大数据的分子进化方法。我们将研究参与氰吸收和合成的基因的获得和损失，比较多面手和那些失去了氰生物合成的基因。总之，这项综合研究将探讨不同昆虫群体使用防御性毒素的生态背景、适应性后果、遗传控制和长期进化轨迹。我们将开发一个易于量化和实验处理的系统，以了解蝴蝶如何对寄主植物化学变化的代谢反应。这对于理解物种如何应对气候变化具有普遍意义。

The evolution of host plant feeding is critical for understanding insect evolution and in particular the responses of populations to a changing climate. For example, UK butterfly species that have done well in response to a warming climate have typically also expanded or altered their patterns of host plant use, while those that have suffered typically have a narrow host plant range. Here we will explore how butterflies can alter their biochemical responses to allow the exploitation of different host plants. This is a form of phenotypic plasticity, where a single genotype can produce alternative phenotypes under different environmental conditions. Plasticity is an important adaptation that can allow organisms to survive variable and heterogeneous environments and promote longer term divergence and diversification. Plant-feeding insects have to deal with toxic plant chemistry, but in some cases such toxins can also provide an important source of defensive chemicals for the insects. Tropical Heliconius butterflies can either obtain cyanogenic toxins from their Passiflora hosts, or can synthesise their own compounds. We have demonstrated that these butterflies can switch between these two strategies dependent on host chemical composition. When the larval diet lacks toxins that can be sequestered, Heliconius respond by increasing biosynthesis of their own defences. This permits use of a wider range of Passiflora species while maintaining their chemical defences. We can readily distinguish toxins derived from the host plant from those that are made by the butterflies, making this an easily quantifiable form of phenotypic plasticity. However, the genetic and biochemical basis of this plasticity remains unknown, as well as it's ecological importance for niche partitioning. We will first address the ecological context, using targeted metabolomics to track the chemical composition of Heliconius erato across seasons at sites with well characterised host plant use in Brazil and Panama. Next, we will explore the fitness trade-offs between different strategies, addressing the reasons for switching between strategies in a plastic species, Heliconius erato. We will compare growth rate and other life history traits of individuals raised on different diets. We will also compare efficiency of sequestration in a derived specialist species, which obtains its toxins only from a specific host plant. Increased efficiency in the derived lineage is predicted by the 'plasticity first' hypothesis. The other major axis of variation for defensive compounds is their influence on predation, and we will measure toxicity and distastefulness of host-plant derived and synthesised toxins. Third, we will explore how plasticity controlled genetically, testing two alternative hypotheses for the molecular control of plasticity. Using transcriptomics we will estimate changes in gene expression in response to larval diet (presence and absence of host-plant derived toxins), and also test whether plasticity is controlled at the level of protein regulation. Finally, we will explore the evolutionary history of cyanogen biosynthesis across the Heliconiines, using molecular evolutionary approaches across a large data of whole genome sequences. We will study the gain and loss of genes involved in cyanogen uptake and synthesis, comparing generalist with those where cyanogen biosynthesis has been lost. In summary, this integrative study will explore the ecological context, fitness consequences, genetic control and long-term evolutionary trajectory of plasticity in the use of defensive toxins across a diverse group of insects. We will exploit a readily quantifiable and experimentally tractable system in order to understand how butterflies respond metabolically to variation in host plant chemistry. This will have general relevance to understanding how species can respond to a changing climate.