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

寄主植物取食的进化对于理解昆虫进化，特别是种群对气候变化的反应至关重要。例如，在应对气候变暖方面表现良好的英国蝴蝶物种通常也会扩大或改变其宿主植物使用模式，而那些遭受影响的蝴蝶通常具有狭窄的宿主植物范围。在这里，我们将探讨蝴蝶如何改变它们的生化反应，以允许利用不同的宿主植物。这是表型可塑性的一种形式，其中单个基因型可以在不同的环境条件下产生替代表型。可塑性是一种重要的适应，它可以使生物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，这种毒素也可以为昆虫提供重要的防御化学物质来源。热带Heliconius蝴蝶可以从它们的西番莲宿主那里获得生氰毒素，或者可以合成它们自己的化合物。我们已经证明，这些蝴蝶可以在这两种策略之间切换，这取决于宿主的化学成分。当幼虫的食物缺乏可以隔离的毒素时，Heliconius通过增加自身防御的生物合成来应对。这允许使用更广泛的西番莲物种，同时保持其化学防御。我们可以很容易地区分来自宿主植物的毒素和蝴蝶产生的毒素，这使得这成为一种易于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仍然未知，以及它的生态位划分的重要性。我们将首先解决生态环境，使用有针对性的代谢组学来跟踪Heliconius erato在巴西和巴拿马具有良好特征的宿主植物使用的地点的化学组成。接下来，我们将探讨不同策略之间的适应度权衡，解决塑料物种Heliconius erato中策略之间切换的原因。我们将比较生长速度和其他生活史性状的个人提出了不同的饮食。我们还将比较衍生的专业物种的螯合效率，该物种仅从特定的宿主植物中获得毒素。“可塑性第一”假说预测衍生谱系的效率增加。防御性化合物的另一个主要变化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不适。第三，我们将探讨可塑性如何控制遗传，测试可塑性的分子控制的两个替代假设。使用转录组学，我们将估计在幼虫的饮食（存在和不存在宿主植物衍生毒素）的基因表达的变化，并测试是否可塑性控制在蛋白质调控的水平。最后，我们将探索氰生物合成的进化历史的Heliconiines，使用分子进化的方法在整个基因组序列的大数据。我们将研究与氰吸收和合成有关的基因的获得和丧失，比较通才与氰生物合成丧失的基因。总之，这项综合研究将探讨生态环境，健身后果，遗传控制和长期的进化轨迹的可塑性在使用防御毒素在不同的昆虫群体。我们将利用一个易于量化和实验处理的系统，以了解蝴蝶如何代谢响应寄主植物化学变化。这将对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.