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

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.

Much of the world's biological diversity was born of and crucially depends upon species interactions. The proposed research will use the interactions between birds and their parasites and mutualists to investigate evolutionary mechanisms and processes generating biodiversity. It will address two main questions: first, what evolutionary processes generate biological diversity within and between interacting species? Second, what genetic mechanisms permit the evolution of specialised adaptations within a single species to multiple coevolutionary partners?

To address these questions, the project will investigate two main model systems. First, antagonistic interactions between hosts and avian brood parasites, which exploit other species to raise their young, leading to coevolutionary arms races between parasitic manipulation (such as egg mimicry) and host defence (such as better egg discrimination). Second, mutualistic interactions between nectar-feeding birds and the specialised plants that depend on them for pollination. Specifically, I will ask: 1. How does frequency-dependent selection generate phenotypic diversity both within and between interacting species, such as egg signatures of identity, and colour polymorphisms in flower colour? 2. How does visual discrimination shape the evolutionary outcome of species interactions, from variation between individuals to properties of entire biological communities? 3. How is specialisation to different coevolutionary partners (such as parasitic host-specificity) genetically maintained within a single species? 4. What is the genetic basis of defensive phenotypic variability (egg 'signatures' of identity) in hosts, and corresponding mimics in parasites?

In answering these questions, the projects will bring together behaviour, visual perception, evolution and diversity, using by way of field experiments, visual modelling, comparative analyses, classical genetics, genomics and transcriptomics.

1. Who will benefit from this research?

1.1. The research will benefit those working in the numerous applied fields to which the coevolutionary process is fundamental. There are particularly clear links with biomedical science (please see 2.1.).

1.2. The research will benefit conservation practitioners and policy-makers.

1.3. The research will benefit practitioners in science education, including preparators of educational materials and museum exhibits.

1.4. The research will benefit innovation in wider society by helping to inspire young people (particularly young women) towards science-related careers.

2. How will they benefit from this research?

2.1. The research will shed further light on the coevolutionary process, which is fundamental to important human challenges such as infectious disease, control of aliens, and pest and disease control in crops. These have clear implications for public health, society and the economy. Mutually beneficial conceptual links with biomedical science are particularly clear, given the close conceptual parallels between diversifying selection from brood parasites on birds' eggs, and diversifying selection from pathogens on tissue antigens (especially those encoded in the major histocompatability complex [MHC]) in adaptive immune systems, including the human immune system. I am currently working on a review paper clarifying these links, in collaboration with an immunologist in the Department of Medicine, University of Cambridge. Moreover, there are clear parallels between the evolution of host-specificity in brood parasites exploiting multiple hosts, and the evolution of pathogens exploiting multiple hosts or host genetic strains.

2.2. The biological richness of ecosystems and the services they provide to humans depend on ecological interactions between species. Species interactions also generate cryptic biological diversity. Basic science leading to a better understanding of the evolutionary mechanisms involved will become more crucial than ever in the face of environmental change. Globalisation and climate change pose a particularly severe threat to species interactions, and hence to healthy ecosystem functioning and the provision of ecosystem services.

2.3. The proposed research is likely to generate vivid examples of the power of natural selection to generate visually striking and easily-appreciated adaptations, with great potential application in science education programmes, including public engagement activities proposed by the applicant (see Pathways to Impact).

2.4. Science is a crucial driver of innovation and the economy. An issue of great concern in the UK is the recruitment of talented young people, and especially young women, to scientific careers. One of the obstacles to overcome is the widespread misconception that scientific careers are stuffy, tedious, and male-dominated. Coevolutionary research in general, and my research on brood parasitic research in particular, has the potential to make a substantial contribution in this regard. The proposed research is vivid, exciting, and easily captures the imagination of the public and young people, and so aids wider understanding and appreciation of science and the dispelling of prejudices about the nature of science and scientists. It has considerable potential to inspire young people, with ultimate benefits to UK society. Science outreach activities will be undertaken by the applicant from the outset of the research programme (see Pathways to Impact).