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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. At the FitzPatrick Institute, three long-term projects address different aspects of this fascinating model system for

Robert Thomson’s team’s work in Finland focusses on how host pairs of Common Redstarts Phoenicurus phoenicurus can completely avoid a Common Cuckoo Cuculus canorus laying an egg in their nest. Hosts that are able to avoid parasites would decrease the fitness costs of parasitism; the earlier that avoidance occurs during the breeding cycle would further minimize these costs. Therefore, adaptations occurring prior to egg laying would be especially beneficial for hosts. The Finnish project investigates frontline 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. Redstarts are the only regular cuckoo hosts that breed in cavities; this aspect challenges adult cuckoos during egg laying and also challenges cuckoo chicks during the phase of evicting host eggs/chicks.

Claire Spottiswoode’s team works in Zambia on three general questions. First, how do interactions between species generate diversity among individuals? Specifically, how do 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 Anomalospiza imberbis and Greater Honeyguides Indicator indicator) in the absence of parasite speciation. Reciprocally, 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 (such as developmental differences and learning) in coevolution? We are interested in how such plasticity might facilitate parasitic exploitation of new host species in the initial absence of appropriate genetic adaptations, and addressing this both within and between species of parasitic finches and honeyguides.

In collaboration with Claire Spottiswoode, Jessie Walton has been studying a population of Brown-backed Honeybirds Prodotiscus regulus which parasitise Karoo Prinias Prinia maculosa at a high rate in the Bot River area of the Western Cape. Among the Brown-backed Honeybirds’ remarkable adaptations that we are investigating are their blue eggs, highly unusual in piciform birds, that broadly mimic those of their hosts. Moreover, up to three honeybird chicks are raised in the same host nest, despite killing host young with their bill hooks. Rob Martin, who founded the honeybird project with Jessie Walton, passed away in May 2017; he is much missed.

Activities in 2017

  • The summer in Finland was one of the coldest in recorded history. Despite lower numbers of breeding birds, an expanded field team monitored the nest boxes and performed several experiments. Highlights included a new collaboration with Dr Rose Thorogood’s team working on egg rejection in the Pied Flycatcher Ficedula hypoleuca and Mira Sassi’s experiment on Redstart behavioural responses to Cuckoos.
  • Two productive field seasons were carried out in Zambia by Gabriel Jamie working on indigobirds and whydahs, and Luke McClean working on honeyguides, both working closely with our team of nest-finders from the Semhawa Farm community.
  • Jessie Walton, assisted by two recent graduates from U. Cambridge, Tanmay Dixit and Jana Riederer, carried out four months of fieldwork on Brown-backed Honeybirds at Bot River.

Highlights:

  • Paper published in Auk about how informed habitat selection as an adaptation against brood parasitism may have implications for brood parasite-host coevolutionary inter-actions (Tolvanen, Forsman and Thomson 2017).
  • Robert Thomson presented at the European Ornithologists Congress in Finland showing for the first time on video how cuckoos lay eggs in cavity breeding host nests.
  • A paper was published in Proceedings of the Royal Society B on how multiple host species affect each other's ever-evolving eggs, with data from the remarkable collection of the late Major John Colebrook-Robjent in Zambia (Caves, Stevens and Spottiswoode 2017). This stimulated an article in The Economist, highlighting the research value of old egg collections.
  • Gabriel Jamie received his PhD (‘Mimicry and speciation in the parasitic finches of Africa’) from U. Cambridge. He will remain in Claire Spottiswoode’s research group as a postdoctoral researcher on the evolutionary genetics of egg colour.
  • Olimpia Onelli passed her PhD thesis examination in the Department of Chemistry at U. Cambridge, supervised by collaborator Dr Silvia Vignolini. Her thesis included a chapter on structural effects of eggshell colour in Brown-backed Honeybird eggs from Jessie Walton’s project at Bot River, and is currently being prepared for publication.
  • Perspectives piece for the journal Science was published on a study by Mary Caswell Stoddard and others, providing a general theory for the evolution and development of egg shape in birds (Spottiswoode, 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 Robert Thomson (FIAO, UCT)
Dr Nicholas Horrocks (U. Cambridge)
Dr Jukka Forsman (U. Oulu, Finland)
Prof. Tomáš Grim (Palacky University, Czech Republic)
Dr Chiara Mrosinoto (U. Padova, Italy)
Prof. Michael Sorenson (U. Boston)
Dr Rose Thorogood (U. Helsinki, Finland)
Jessie Walton (FIAO, UCT)

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

Research assistants:
Finland: Claire Buchan, Felicias Pamatat, Shu Shan.
Zambia: Silky Hamama, Lazaro Hamusikili, Oliver Kashembe, Kiverness Moono, Collins Moya, Gift Muchimba, Sylvester Munkonka, Oliver Munsaka, Sanigo Mwanza, Calisto Shankwasiya and many
others.
South Africa: Tanmay Dixit, Jana Riederer.

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