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.

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. This project also studies whether cuckoo females use behaviour and physiology to enhance the manipulative signals that cuckoo nestlings use to extract as much care as possible from their foster parents.

Claire Spottiswoode’s team works on a variety of brood-parasitic systems in Zambia, focusing mainly on three broad 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 Prof. Michael Sorenson (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. 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 2022

  • Robert Thomson was finally able to get to the field in Finland where he spent some weeks working with University of Helsinki PhD student Teresa Abaurrea, investigating whether cuckoo chicks use carotenoid-based signals to manipulate their foster parents. Prof Rose Thorogood’s assembled team were able to continue the long-term monitoring of the cuckoo parasitism on the redstart population.
  • Teresa Abaurrea successfully conducted her second fieldwork season of her PhD in Oulu with the help of Ronja Saarinen and Justine Loof who also conducted their own projects for their MSc and undergraduate theses respectively.
  • Teresa presented the results of the first chapter of her thesis at the LUOVA Spring Symposium, and at the 18th conference of the International Society for Behavioural Ecology, organised in Stockholm.
  • Cameron Blair joined the team for his MSc research at the Fitz, studying how honeyguide chicks acoustically manipulate their foster parents into feeding them more.
  • After the Covid hiatus, it was wonderful to resume two full seasons of fieldwork in Zambia: rainy season fieldwork in February–March (Cameron Blair, Dr Gabriel Jamie and Jonah Walker, together with Maggie Mwale from Livingstone Museum), and dry season fieldwork in September–November (Cameron Blair, Jess Lund and Mairenn Attwood), working on cuckoo finches, honeyguides, African cuckoos and their hosts, together with our local field team led by Collins Moya and Silky Hamama.
  • Gabriel Jamie carried out a successful season of wide-ranging fieldwork across Zambia, as part of his Leverhulme Early Career Research Fellowship in which he is exploring the evolution of polymorphisms across the Cisticolidae family which exhibit some of the most complex and diverse eggs of any group of birds in the world.

Highlights

  • Angela Moreras, Robert Thomson and several collaborators published a paper in Oecologia exploring if territory location decisions prior to breeding to associate with other species of the forest bird community may have implications for brood parasitism risk.
  • After a PhD where her field data collection was completely cancelled by Covid restrictions, Angela Moreras continued to work on various questions investigating frontline strategies used by redstarts to counter cuckoo brood parasitism and finished her thesis in the last days of 2022.
  • Claire Spottiswoode, Gabriel Jamie and key collaborator Prof Michael Sorenson (Boston University) and others, including chief fieldworkers Collins Moya and Silky Hamama published a paper in Proceedings of the National Academy of Sciences of the USA which addressed the long-standing puzzle of how exquisite mimicry of the eggs of several different host species can evolve within a single species of brood-parasitic bird. They showed that in Cuckoo Finches in Zambia, egg mimicry of different host egg phenotypes is maternally inherited, which allows mothers to transmit host-specific adaptations to their daughters irrespective of which host species the father was raised by. This has allowed egg mimicry of multiple hosts to evolve and remain distinct within Cuckoo Finch matrilines, that we found have been perfectly host-specific for up to two million years or more. However, we suggest that maternal inheritance is in fact a double-edged sword for parasites, because it appears to hamper further adaptation in coevolutionary arms races with their hosts, which we show to inherit egg appearance from both parents.
  • In a collaboration between biologists and computer scientists, Tanmay Dixit, Claire Spottiswoode and collaborators at the University of Cambridge published a paper in Proceedings of the Royal Society of London B on the evolution of pattern complexity in birds’ eggs. They used machine learning to compute a biologically-relevant measure of egg pattern complexity, and combined this with field experiments in Zambia to investigate how complexity evolves in an arms race between host egg signatures (by Tawny-flanked Prinias Prinia subflava) and parasitic egg forgeries (by Cuckoo Finches). They found that pattern complexity predicted whether foreign eggs were accepted in prinia nests or accepted as one of the host’s own, and that cuckoo finch eggs have simpler patterns to prinia eggs, suggesting that high complexity in prinia egg patterns has evolved to make forgery of these ‘signatures’ difficult.
  • Claire Spottiswoode, Jess Lund and David Lloyd-Jones published a “Quick Guide” on honeyguides in Current Biology, celebrating their fascinating lives as both brutal brood parasites of other birds and mutualistic partners of our own species.
  • Silky Hamama, chief fieldworker at our Choma field site in Zambia, presented a poster on nest access techniques for research at the Pan-African Ornithological Congress in Victoria Falls. Together with Claire Spottiswoode, he also co-presented as part of a Round Table discussion on involving local communities in research.
  • Cameron Blair, Jess Lund and Mairenn Attwood also gave talks at the Pan-African Ornithological Congress, sharing findings from their prior Honours and Masters research on brood parasites, involving Greater Honeyguides, African Cuckoos, and their respective hosts in Zambia.
  • The Zambia brood parasite team continued their diverse outreach and collaborative activities internationally, including presenting talks to schools in both Zambia and the UK. Tanmay Dixit was a founding co-presenter of the “Evolution Crash Course” online course for students in the Global South. Gabriel Jamie spent two months teaching and mentoring at the AP Leventis Ornithological Research Institute in Jos, Nigeria.

Key co-supporters
Biotechnology and Biological Sciences Research Council; The Leverhulme Trust; Societas pro Fauna et Flora Fennica; Finnish Cultural Foundation; LUOVA Doctoral Programme in Wildlife Biology at the University of Helsinki.

Research team 2022
Prof. Claire Spottiswoode (FIAO, UCT / U. Cambridge)
A/Prof. Robert Thomson (FIAO, UCT)
Dr Gabriel Jamie (U. Cambridge/FIAO, UCT)
Prof. Michael Sorenson (Boston University)
A/Prof. Rose Thorogood (U. Helsinki, Finland)
Dr Jere Tolvanen (U. Oulu, Finland)
Jonah Walker (U.Cambridge)
Jessie Walton (FIAO, UCT)

Students: Finland: Teresa Abaurrea (PhD, U. Helsinki); Angela Moreras (PhD, UCT); Ronja Saarinen (MSc, U. Helsinki); Justine Loof (undergraduate student, Institut AgroDijon, Université Bourgogne Franche-Compté); Zambia: Mairenn Attwood (PhD, Cambridge); Cameron Blair (MSc, UCT); Tanmay Dixit (PhD, Cambridge); Jess Lund (PhD, Cambridge)

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