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Coevolutionary arms races in brood parasites and their hosts

Coevolution is the process by which two or more species influence each other’s evolution. Brood-parasitic birds, the cheats of the bird world, give us an ideal opportunity to study coevolution in the wild. Coevolutionary “arms races” arise when 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 works 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 parasitising their nest. Hosts that are able to avoid parasites decrease the fitness costs of parasitism; the earlier that avoidance occurs during the breeding cycle, the lower the cost. Therefore, host adaptations before egg laying would be especially beneficial. The Finnish project investigates the redstart’s frontline defences (nest site choice, habitat selection, nest building decisions) and the cuckoo’s counter-adaptations (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 maintained? The genetic basis of signature-forgery arms races is almost entirely unknown. In collaboration with Michael Sorenson, 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. We are also interested in the genetic basis of host defences, and whether convergent genetic mechanisms have evolved in their parasitic mimics. Third, what is the role of phenotypic plasticity (such as developmental differences and learning) in coevolution, and how might such plasticity facilitate exploitation of new host species in the absence of appropriate genetic adaptations? We are addressing this question for indigobirds, whydahs and honeyguides.

Fitz Research Associate Jessie Walton has been studying 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 2020

  • The field season in Finland had to be abandoned due to COVID-19 travel restrictions; even the project’s in-country collaborators were unable to visit the field site. Existing long-term project datasets were used by Angela Moreras and new PhD student Teresa Abaurrea during the year to explore potential interspecific protection against cuckoo parasitism and cuckoo host choice.
  • In Zambia, we were able to carry out two-thirds of a productive rainy season before the COVID-lockdowns forced our team to hurry home. Tanmay Dixit carried out further egg rejection experiments on Cuckoo Finch hosts towards his PhD, and helped facilitate Stephanie McClelland, a visiting student from Royal Holloway (U. London), working on embryonic physiology of brood-parasitic birds.
  • Post-doc Gabriel Jamie completed sampling to construct a high-quality genome of one of our main Zambian study species, the Tawny-flanked Prinia Prinia subflava, to enable an understanding of the genetic basis of its remarkable egg ‘signatures’ that have evolved as defences against brood parasitism.
  • Unfortunately, dry season fieldwork in Zambia was impossible, but Jess Lund (honeyguides and their hosts) and Mairenn Collins Attwood (Fork-tailed Drongos Dicrurus adsimilis and African Cuckoos Cuculus gularis) look forward to returning in 2021 to begin their PhD fieldwork.
  • During much of 2020 the research team focussed on data analysis and writing, drafting several manuscripts and preparing conference presentations.

Highlights

  • Luke McClean (UCT) graduated with his PhD entitled “Coevolution between brood-parasitic honeyguides and their hosts”, which included five chapters that he is now preparing for publication.
  • Mairenn Attwood (Cambridge) graduated with her MPhil entitled “Angry birds: does it pay a cuckoo to parasitise a highly aggressive host?” which included three chapters that she is now preparing for publication.
  • Masters students Jess Lund (UCT) and Mairenn Attwood (Cambridge) were each awarded PhD scholarships at the University of Cambridge, and will both continue their research on brood parasites and their hosts in Zambia during their PhDs from 2021.
  • Gabriel Jamie, Claire Spottiswoode, Silky Hamama, Collins Moya and collaborators published a paper in Evolution showing how indigobirds and whydahs mimic the chicks of their specialist host species visually, vocally and with respect to their begging movements. This sheds light on how imprinting and mimicry have promoted sympatric speciation in indigobirds and whydahs. The research featured on the journal’s cover.
  • Gabriel Jamie published a review paper with Joana Meier in Trends in Ecology and Evolution exploring the phenomenon that the same polymorphisms often recur in many members of a species radiation. The paper was chosen as the  editor’s “Pick of the Month” and featured on the journal cover.
  • CB MSc student Rowan Hickman collaborated with chief field assistant Collins Moya to identify all the bird calls on her sound recordings from northern Zambia as part of her research project on the effect of mining on miombo birds.
  • We launched our revamped project website at www.AfricanCuckoos.com.

Key co-supporters
Biotechnology and Biological Sciences Research Council; The Leverhulme Trust: Societas pro Fauna et Flora Fennica; Finnish Cultural Foundation

Research team 2020
Prof. Claire Spottiswoode (FIAO, UCT / U. Cambridge)
Dr Robert Thomson (FIAO, UCT)
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: Teresa Abaurrea (PhD, U. Helsinki); Tanmay Dixit (PhD, Cambridge); Luke McClean (PhD, UCT); Angela Moreras (PhD, UCT); Mairenn Attwood (MPhil, Cambridge); Jess Lund (MSc, UCT); Rowan Hickman (CB MSc, UCT).

Research assistants
Zambia: Silky Hamama, Lazaro Hamusikili, Oliver Kashembe, Kiverness Moono, Collins Moya, Gift Muchimba, Sylvester Munk`onko, Sanigo Mwanza, Calisto Shankwasiya and many others.