Evolution and ecology of extractive foraging in birds and mammals

提取式觅食是定位和加工嵌入或包裹食物的行为，如地下植物储存器官、蛀木节肢动物、贝类或由多刺、坚韧或坚硬基质保护的植物部分。它被认为可以提高动物利用资源的效率，使它们能够在不适宜居住的环境中生存，但令人惊讶的是，对其大规模进化和生态后果的研究却很少。鸟类和哺乳动物已经进化出了各种各样的特化特征，以实现采掘性觅食，包括特定的形态，如食蚁兽的长鼻子、长舌头和弯曲的前爪，以及特定的行为，如类人猿和新喀里多尼亚乌鸦等类群所表现出的听觉引导的挖掘和工具使用。类似的觅食适应性，如鸟类和灵长类动物的双目视觉，似乎在不同的分类群中独立进化了多次，但这些趋同进化的潜在案例尚未得到正式研究。我们对采掘性觅食和工具使用之间的进化关系也知之甚少：前者是否更倾向于后者，如果在什么条件下会这样？尽管具有潜在的优势，但在鸟类和哺乳动物中，提取性觅食在系统发育上是零星分布的，这表明它只在特定条件下进化，而且这种条件在生命树的各个独立案例中反复出现。这些重现提供了一个使用系统发育比较方法的机会，不仅可以检查有利于提取觅食的生态条件，如饮食类型和季节性，还可以检查形态学因素，其出现的限制，以及其对行为，生态位占用，进化速率和物种形成的进化反馈效应。例如，目前尚不清楚是什么条件有利于特定行为（如工具使用与特定形态），也不清楚这种行为出现后对种群动态、支系多样化和进化速度的影响。复杂的采掘觅食行为模式被认为是认知上的要求，需要长期的发展来促进学习，预测复杂的采掘觅食行为与大脑大小或结构、成熟年龄、幼年期和非社交游戏时间之间的联系。采掘性觅食可以缓冲个体对环境扰动的影响，预测采掘性觅食与环境不可预测性或季节性之间的联系。我们将测试大脑大小进化的“提取性觅食假说”，该假说表明，在没有特殊形态的情况下，提取性觅食与感觉运动技能和大脑大小有关。我们将在鸟类和哺乳动物这两种进化了多次的进化分支中研究这些问题，并研究在每种进化分支中观察到的模式的相似之处和差异。该项目将使用最近开发的系统发育方法，允许对进化变化的模式和过程进行推断，使我们能够解决四个主要问题：(i)特征之间的相关进化，包括行为，神经解剖学和认知；（ii）进化序列，使用定向方法，检验因果假设和检查诸如采掘觅食和/或工具使用行为是否与在系统发育分支上获得的行为同样可能丢失，以及这些行为在最初出现后是否倾向于增加复杂性等问题；（iii）与采掘觅食和工具使用相关的进化变化率及其可变性（例如，这种行为的出现是否增加或减少了形态和/或行为的变化率）；（iv）采掘觅食的出现、种群密度、新生态位的入侵和物种形成之间的关系

Extractive foraging is the act of locating and processing embedded or encased foods such as underground plant storage organs, wood-boring arthropods, shellfish or plant parts protected by a thorny, tough or hard matrix. It is assumed to enhance the efficiency with which animals can exploit resources, enabling them to inhabit otherwise inhospitable environments, but its large-scale evolution and ecological consequences have been surprisingly little studied. A variety of specializations have evolved in birds and mammals to enable extractive foraging, including both specialised morphologies such as the elongated snouts and tongues and curved foreclaws of anteaters, and specialised behaviours, such as the auditorily-guided excavation seen in aye-ayes and tool-use displayed by taxa such as great apes and New Caledonian crows. Similar adaptations for extractive foraging, such as binocular vision in birds and primates8-9 appear to have evolved multiple times independently in different taxa, but these potential cases of convergent evolution have not been formally studied. We also know little about the evolutionary relationship between extractive foraging and tool use: does the former predispose to the latter, and if so under what conditions? Despite its potential advantages, extractive foraging is phylogenetically patchily distributed across birds and mammals, suggesting that it evolves under only certain conditions, and that such conditions have recurred repeatedly in independent cases, across the tree of life. These recurrences provide an opportunity to use phylogenetic comparative methods to examine not only the ecological conditions favouring extractive foraging, such as diet type and seasonality, but also morphological predisposing factors, constraints on its emergence, and its evolutionary feedback effects on behaviour, niche occupancy, evolutionary rates and speciation. For example, the conditions favouring specialised behaviours such as tool-use versus specialised morphologies are currently unknown, as are the effects on population dynamics, clade diversification and evolutionary rates after it appears. Complex patterns of extractive foraging behaviour are thought to be cognitively demanding and require extended development to facilitate learning, predicting associations between complex extractive foraging, brain size or structure, age at maturity, juvenile period and amount of time spent in non-social play. Extractive foraging may buffer individuals against environmental perturbations, predicting associations between extractive foraging and environmental unpredictability or seasonality. We will test the "Extractive foraging hypothesis" for brain size evolution, which suggests that extractive foraging in the absence of specialised morphology is associated with sensory-motor skills and brain size. We will examine these questions in two clades within which extractive foraging has evolved multiple times, birds and mammals, and examine the parallels and differences in the patterns observed within each. This project will use recently developed phylogenetic methods that permit inference of the patterns and processes of evolutionary change, allowing us to address four major questions: (i) Correlated evolution between traits, including behaviour, neuroanatomy and cognition; (ii) Evolutionary sequences, using directional methods, to test causal hypotheses and examine questions such as whether extractive foraging and/or tool using behaviour is equally likely to be lost as gained on phylogenetic branches and whether these behaviours tends to increase in complexity after their initial emergence; (iii) Rates of evolutionary change and their variability in relation to extractive foraging and tool use (e.g. does the emergence of such behaviours increase or decrease rates of change in morphology and/or behaviour); (iv) Relationships between emergence of extractive foraging, population density, invasion of new niches, and speciation