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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. Three long-term projects address different aspects of this fascinating model system for coevolution.

Robert Thomson’s team work in Finland, where their research focuses 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, host adaptations occurring prior to egg laying would be especially beneficial, because the host's entire clutch is preserved if frontline defences are successful. The Finnish project investigates these frontline defences (nest site choice, habitat selection, nest building decisions) and the counter-adaptations by parasites (prospecting and laying strategies), which have received little attention to date. Redstarts are the only regular cuckoo host that breeds in cavities which makes it difficult for female cuckoos to lay eggs and for their newly-hatched chicks to evict host eggs/chicks.

Claire Spottiswoode’s team works in Zambia on three 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 (e.g. 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. The remarkable adaptation that we are investigating is 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 2019

  • Angela Moreras joined the project as a PhD student. Her first task was to lead the Finnish field season where she collected long-term data on Redstart nest location, decisions and parasitism rates while also doing a field experiment that manipulated Redstart nest parasitism vulnerability and measured behavioural responses.
  • Justin Jacobs investigated prospecting of Common Cuckoos at Redstart nests as part of his UCT BSc Hons thesis. This rarely reported behaviour in brood parasites was surprisingly common in the study system.
  • In the rainy season in Zambia, Gabriel Jamie completed sampling on the genetic basis of egg signatures in Tawny-flanked Prinias. Tanmay Dixit began PhD field research on the evolution of prinia egg signatures and Cuckoo Finch egg forgeries. Tanmay and Jess Lund hosted Stephanie McClelland, a PhD student from Royal Holloway (U. London).
  • Two new students began MSc research on coevolution between Fork-tailed Drongos Dicrurus adsimilis and their African Cuckoo Cuculus gularis parasites: Jess Lund is studying the genetic and phenotypic consequences of egg signatures in drongos and Mairenn Collins Attwood is studying hawk mimicry by African Cuckoos.
  • After four seasons of fieldwork in Zambia, Luke McClean completed writing up his PhD entitled “Coevolution between brood-parasitic honey-guides and their hosts” which reveals some fascinating adaptations and counter-adaptations.

Highlights

  • Gabriel visited our colleagues at Copperbelt University in Kitwe, Zambia, to share our research findings and plan future collaborative activities. He gave several outreach talks at schools and science festivals in Zambia and the UK.
  • The special issue of Philosophical Transactions of the Royal Society of London B co-edited by Claire Spottiswoode titled “The coevolutionary biology of brood parasitism: from mechanism to pattern” was published in February.
  • This special issue contained two empirical papers from our Zambian project: “Higher-level pattern features provide additional information to birds when recognizing and rejecting parasitic eggs” and “Convergent evolution of reduced eggshell conductance in avian brood parasites”.
  • It also contained two theoretical review papers part-inspired by our work in Zambia: “Vive la difference! Self/non-self recognition and the evolution of signature polymorphism in arms races with parasites” and “The coevolutionary biology of brood parasitism: a call for integration”.
  • Claire presented recent highlights from our Zambian project at the “Frontiers in Behavioural Research” symposium at the Max Planck Institute for Ornithology, Seewiesen, Germany.

Key co-supporters
European Research Council; National Geographic Society; Max Planck Institute for Evolutionary Anthropology; DST-NRF CoE grant; British Ecological Society; Association for the Study of Animal Behaviour; American Ornithological Society.

Research team
Prof. Claire Spottiswoode (FIAO, UCT and U. Cambridge)
Dr Robert Thomson (FIAO, UCT)
Dr Diana Bolopo (FIAO, UCT)
Dr Nicholas Horrocks (U. Cambridge)
Dr Gabriel Jamie (U. Cambridge)
Prof. Michael Sorenson (Boston University)
Dr Rose Thorogood (U. Helsinki, Finland)
Dr Jere Tolvanen (U. Oulu, Finland)
Jessie Walton (FIAO, UCT)

Students: Tanmay Dixit (PhD, Cambridge); Luke McClean (PhD, UCT); Angela Moreras (PhD, UCT); Mairenn Collins Attwood (MPhil, Cambridge); Jess Lund (MSc, UCT); Justin Jacobs (BSc Hons, UCT).

Research assistants:
Finland: Joshua Strauss.
Zambia: Silky Hamama, Lazaro Hamusikili, Oliver Kashembe, Kiverness Moono, Collins Moya, Gift Muchimba, Sylvester Munkonka, Sanigo Mwanza, Calisto Shankwasiya and many others.