Species interactions and the evolution of biological diversity: visual signalling in antagonistic and mutalistic coevolution

世界上大部分的生物多样性都是由不同物种之间的相互作用产生的，而且在很大程度上取决于不同物种之间的相互作用。它们为我们提供了一些自然界中最令人惊讶的适应例子：杜鹃蛋完美地模仿了宿主的蛋，或者长舌蝇为长刺兰花授粉。这些都是共同进化的产物，这是两个或多个物种相互影响彼此进化的过程。但是，共同进化不仅是产生生物多样性的强大力量：它对人类面临的挑战至关重要，例如保护生态系统及其为我们提供的服务、生物防治以及不断变化的传染病和耐药性威胁。为了应对这些挑战，我们需要彻底了解所涉及的进化机制。该项目旨在通过研究鸟类与它们对抗的拮抗者（它们的幼虫寄生虫）以及它们合作的互惠者（它们授粉的植物）之间的相互作用，更好地理解共同进化和产生生物多样性的过程。物种之间的相互作用在热带地区是最古老的，在那里它们可能最能揭示一般的进化过程。因此，我的寄生研究将利用在赞比亚研究的三种独立进化的热带育雏寄生系统。像杜鹃这样的幼虫寄生虫是鸟类世界的骗子，它们利用其他物种的照顾来抚养它们的后代。它们可能陷入与宿主的共同进化军备竞赛中，因为寄生虫进化得越来越好，可以更好地操纵宿主（比如模仿宿主的卵），而宿主也会做出更精细的防御（比如拒绝模仿宿主的卵）。在这个项目中，我将首先询问物种之间的相互作用如何在个体之间产生多样性，以及这是如何由视觉感知形成的。杜鹃雀和赞比亚的非洲杜鹃参与了鸟蛋外观的生物军备竞赛，不同的寄主雌性不断进化出新的蛋类型，以逃避追逐寄生虫的模仿。我将问宿主如何使它们的卵最难被模仿（就像纸币上的水印可以阻止伪造者一样），不同的宿主如何影响彼此的多样化，以及当寄生虫几乎完美地伪造卵子时，进化是如何进行的。为了做到这一点，我将在宿主的巢穴进行实地实验，并结合计算机视觉建模，通过鸟类的眼睛来表达鸡蛋的外观，因为鸟类的视觉比我们自己的视觉要好。然后，我将问是否类似的过程可能在互惠的相互作用中运作：我将测试鸟类传粉者的视觉辨别是否有利于靠近彼此开花的物种之间的颜色差异或趋同，从而导致同一物种的植物在不同的当地群落之间多样化。其次，我将试图解决宿主-寄生虫研究中一个存在了几个世纪的难题：同一物种的不同雌性幼虫寄生虫如何在与其他宿主饲养的雄性寄生虫杂交的情况下，产卵模仿它们所选择的宿主？一种假设是，这些特殊的适应性仅通过雌性特有的鸟类W染色体遗传给雌性。在赞比亚，我们发现寄生雌性的谱系在数百万年的时间里对它们选择的宿主完全忠诚，这可能使这种专门化的进化成为可能。我建议通过定位参与不同宿主物种和不同宿主特征的模仿的基因来验证这一点。我将通过圈养布谷鸟的繁殖实验，结合先进的DNA测序和对卵子形成的输卵管中基因表达的研究来做到这一点。最后，我将定位参与产生复杂卵子特征的宿主基因，以揭示相似的遗传机制是否在宿主及其如此美丽地模仿它们的寄生虫中趋同进化。

Much of the world's biological diversity was born of and crucially depends upon interactions between different species. They give us some of the most astonishing examples of adaptation seen in nature: a cuckoo egg perfectly mimicking that of its host, or a long-tongued fly pollinating a long-spurred orchid. These are products of coevolution, which is the process by which two or more species reciprocally influence one another's evolution. But coevolution is not only a potent force in generating biodiversity: it is crucial to human challenges such as conservation of ecosystems and the services they provide us, biocontrol, and the ever-changing threat of infectious disease and drug resistance. To address these challenges, we need a thorough understanding of the evolutionary mechanisms involved.This project aims better to understand coevolution and the processes generating biological diversity by studying the interactions between birds and the antagonists they battle against (their brood parasites), and the mutualists they cooperate with (the plants they pollinate). Interactions between species are at their most ancient in the tropics, where they might be most revealing of general evolutionary processes. My parasitic research will therefore exploit three independently evolved tropical brood parasitic systems studied in Zambia. Brood parasites such as cuckoos are the cheats of the bird world, that exploit the care of other species to raise their young. They can become locked in coevolutionary arms races with their hosts, as parasites evolve ever better manipulation of hosts (such as mimicry of host eggs), and hosts respond with ever more refined defences (such as rejecting mimetic eggs).In this project, I will first ask how interactions between species can generate diversity among individuals, and how this is shaped by visual perception. The Cuckoo Finch and African Cuckoo in Zambia are involved in biological arms races in bird egg appearance, whereby different host females are continually evolving new egg types to escape mimicry by their pursuing parasite. I will ask how hosts might make their eggs most difficult to mimic (just as the watermarks of banknotes deter forgers), how different hosts might affect one another's diversification, and how evolution proceeds when parasites achieve almost perfect egg forgeries. To do so I will carry out field experiments at hosts nests, together with computer modelling of vision in order to express egg appearance through a bird's eye, since birds vision is superior to our own. I will then ask whether similar processes might operate in mutualistic interactions: I will test whether visual discrimination by bird pollinators favours flower colour divergence or convergence between species flowering near one another, and thus cause plants of the same species to diversify between different local communities.Second, I will attempt to solve a centuries-old conundrum for host-parasite research: how do different female brood parasites of the same species lay eggs that mimic those of their chosen host, despite interbreeding with males raised by other hosts? An hypothesis is that these specialised adaptations are inherited in the female line alone, via the female-specific avian W chromosome. In Zambia we have discovered that lineages of parasitic females have stayed perfectly faithful to their chosen hosts for millions of years, which could allow such specialisation to evolve. I propose to test this by locating the genes involved in mimicry of different host species and different host signatures. I will do so by way of breeding experiments on captive Cuckoo Finches, in combination with advanced DNA sequencing and studies of gene expression in the oviduct where eggs are formed. Finally, I will locate the host genes involved in generating complex egg signatures, to reveal whether similar genetic mechanisms have convergently evolved both in hosts and their parasites that so beautifully mimic them.