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Coevolutionary arms races in brood parasites and their hosts

Coevolution is the process by which two or more species reciprocally influence one another’s evolution, and can escalate to produce beautifully refined adaptations. Brood-parasitic birds, the cheats of the bird world, give us an ideal opportunity to study coevolution in the wild. Coevolutionary “arms races” can arise as hosts evolve defences such as rejecting parasitic eggs, which imposes natural selection for parasitic counter-adaptations such as mimicry of host eggs, and in turn for ever more sophisticated defences from hosts. Two long-term projects address different aspects of this fascinating model system for coevolution: Claire Spottiswoode’s and her team study a range of African brood parasites (including cuckoos, honeyguides and parasitic finches such as Cuckoo Finches, indigobirds and whydahs) in Zambia; and Robert Thomson and his team study the Common Cuckoo Cuculus canorus and its host the Common Redstart Phoenicurus phoenicurus in Finland.

Claire Spottiswoode’s team in Zambia focuses on three general questions: first, how do interactions between species generate diversity among individuals? We are interested in how biological arms races between hosts and parasites shape phenotypic diversity in both parties. For example, parasites diversify to mimic multiple hosts, and in response hosts sometimes diversify with defensive adaptations to foil mimicry, such as visual 'signatures' of identity. Second, how is specialisation to different coevolutionary partners genetically maintained? The genetic basis of signature-forgery arms races played out by brood parasitic birds is currently almost entirely unknown. In collaboration with Prof. Michael Sorenson and his lab at Boston University, we are using genomic approaches to ask how specialised adaptations to different host species (mimicry of host eggs) are maintained within a single parasitic species (Cuckoo Finches and greater honeyguides) in the absence of parasite speciation. We are also investigating the mechanistic basis of host-specific adaptation in specialist brood parasites that have speciated to parasitise one species each (the Vidua finches: whydahs and indigobirds). We are also interested in the genetic basis of host defences, and whether convergent genetic mechanisms have evolved in their corresponding parasitic mimics. Third, what is the role of phenotypic plasticity in the coevolutionary process? We are interested in how phenotypic plasticity might facilitate parasitic exploitation of new host

species in the initial absence of appropriate genetic adaptations. Such a role for plasticity in facilitating novel adaptations would imply that, contrary to the long-established paradigm,  environmentally-induced variation might some-times shape the course of subsequent genetic evolution. We are addressing these questions both within and between species of parasitic finch.

Robert Thomson’s team in Finland focusses on the evolution of front-line defences in hosts: how can host pairs stop a cuckoo laying an egg in their nest? Much work on brood parasitism has focussed on host adaptations and parasite counter-adaptations during the egg-laying phase, but recently the emphasis has been extended to cover all stages of the host breeding cycle. Hosts that are able to avoid parasites decrease the fitness costs of parasitism; these costs would be further reduced the earlier

during the breeding cycle that avoidance occurs. Therefore, adaptations occurring prior to egg laying would be especially beneficial for hosts. The Finnish project investigates defences used by hosts and counter-adaptations by parasites, especially during nest site and territory location decisions, which have received almost no attention to date. Common Redstarts are the only regular cuckoo hosts that breed in cavities, which challenges adult cuckoos during egg laying and makes it harder for cuckoo chicks to evict host eggs/chicks. This project further investigates habitat selection decisions that allow hosts to associate with heterospecifics in the bird community as an adaptation to decrease parasitism rates.

Activities in 2016

  • Two 3-month field seasons were performed by the Zambian team: PhD student Gabriel Jamie working on indigobirds and whydahs and Claire Spottiswoode working on Cuckoo Finches during the rainy season, and MSc student Luke McClean working on honey-guides during the dry season.
  • Gabriel Jamie presented his finding on Vidua-host interactions in a very well-received talk at the International Society for Behavioral Ecology congress in Exeter, UK, in July 2016.
  • PhD student Michal Kysučan visited the Fitz for 3 months to work on a key paper in the project. Prof Tomáš Grim also visited for 3 weeks.
  • A 3-month northern summer field season was performed by the Finland team.

Highlights:

  • Paper published on range changes in South African brood parasites and their hosts, in collaboration with the Statistics in Ecology, Environment and Conservation group at UCT (Péron et al. 2016. J.Anim. Ecol.)
  • Paper published describing the uniqueness of the redstart-cuckoo system (Thomson et al. 2016. J. Avian Biol.)
  • Paper published on migration of young Common Cuckoos to Africa, using cuckoo chicks followed in the Finnish study system (Vega et al. 2016. PLoS One)
  • Luke McClean received a MSc Study Abroad Studentship from The Leverhulme Trust to study honeyguide-host interactions in Zambia, supervised by Claire Spottiswoode and Nick Horrocks.
  • A film crew making a documentary for German national television successfully filmed honeyguide-host interactions at our study site in Zambia.
  • Our honeyguide-host research was featured in the prime-time BBC program 'World's sneakiest animals' with presenter Chris Packham, and is available internationally on the Discovery Channel.
  • Dr Chiara Morosinotto received a Post-doc fellowship from the Finnish Cultural Foundation to work in the project for 12 months in 2017.

Key co-sponsors

DST-NRF CoE grant; Academy of Finland; Finnish Cultural Foundation, University of Oulu graduate School; Biotechnology and Biological Sciences Research Council (BBSRC); The Leverhulme Trust.

Research team

Prof. Claire Spottiswoode (FIAO, UCT and U. Cambridge)
Dr Nicholas Horrocks (U. Cambridge)
Prof. Michael Sorenson (U. Boston)
Dr Robert Thomson (FIAO, UCT)
Dr Jukka Forsman (U. Oulu, Finland)
Prof Tomáš Grim (Palacky University, Czech Republic)

Students: Gabriel Jamie (PhD, U. Cambridge), Jere Tolvanen (PhD, Oulu); Michal Kysučan (PhD, Palacky) Luke McClean (MSc, UCT)

Research assistants: Charles Banda, Silky Hamama, Lazaro Hamusikili, Oliver Kashembe, Kiverness Moono, Collins Moya, Gift Muchimba, Austin Muleya, Refi Munkombwe, Sylvester Munkonka, Oliver Munsaka, Sanigo Mwanza, Sunnyboy Mwanza, Calisto Shankwasiya, Danny Siyapolo.