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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 coevolution.

Robert Thomson’s team work in Finland focusing on how host pairs of Common Redstarts Phoenicurus phoenicurus can decrease the chance of 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.

Fitz Research Associate 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. How honeybirds escape being killed by their nestmates remains an intriguing mystery.

Activities in 2018

  • The field season in Finland continued with a smaller than usual field team which focused on continuing the long-term data on redstart nest location decisions and their parasitism rates.
  • In the rainy season in Zambia, Dr Gabriel Jamie completed sampling for his research on the genetic basis of egg signatures in Tawny-flanked Prinias; sequencing is now underway. Interns Tanmay Dixit and Jana Riederer successfully carried out projects on Cuckoo Finch-host interactions, and Tanmay began his PhD on this topic at the University of Cambridge later in 2018.
  • In the dry season in Zambia, Luke McClean completed his final season of field experiments on honeyguide-host interactions before writing up his PhD, and hosted a visiting PhD student from Royal Holloway University of London.
  • In the Cape spring, Jessie Walton carried out a successful field season on Brown-backed Honeybirds.

Highlights

  • Jere Tolvanen defended and received his PhD entitled ‘Informed habitat choice in the heterogeneous world: ecological implications and evolutionary potential’.
  • Amongst other outreach activities in Zambia, Gabriel Jamie and the field team hosted the Livingstone Museum’s newly-appointed ornithologist, Maggie Mwale, at our field site for a week and assisted with capacity building.
  • Gabriel Jamie was a selected speaker at the Joint Congress on Evolutionary Biology, Montpellier, France, giving a talk on indigobird and whydah speciation.
  • Claire Spottiswoode co-edited a special issue of Philosophical Transactions of the Royal Society of London B, entitled “The co-evolutionary biology of brood parasitism: from mechanism to pattern” (published Feb 2019).

Key supporters
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 Gabriel Jamie (U. Cambridge)
Dr Jukka Forsman (U. Oulu, Finland)
Prof. Michael Sorenson (U. Boston)
Dr Rose Thorogood (U. Helsinki, Finland)
Jessie Walton (FIAO, UCT)

Students: Jere Tolvanen (PhD, Oulu); Tanmay Dixit (PhD, Cambridge); Luke McClean (MSc, UCT); Mira Sassi (MSc, Oulu)

Research assistants:
Finland: Finland: Carles Dura, Verity Bridger, Vicky Pritchard.
Zambia: Silky Hamama, Lazaro Hamusikili, Oliver Kashembe, Kiverness Moono, Collins Moya, Gift Muchimba, Sylvester Munkonka, Sanigo Mwanza, Calisto Shankwasiya and many others.