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Unravelling an extended phenotype: sexual selection and the evolution of nest architecture in weaverbird defence against brood parasitism

Periodic Reporting for period 2 - WEAVERBIRD_DEFENCE (Unravelling an extended phenotype: sexual selection and the evolution of nest architecture in weaverbird defence against brood parasitism)

Reporting period: 2021-07-08 to 2022-07-07

Why is nature so diverse? In the natural world, the same problems recur but nature’s solutions manifest in strikingly different forms. As evolutionary biologists, we are interested in understanding the processes and mechanisms that lead to this variation. And increasingly, as scientists and as a society, we are turning to nature for inspiration to solve human problems and to counteract the consequences of human activity.

One dominant force in nature is coevolution, which often leads to escalating arms races of adaptations and counteradaptations. Cuckoos and their hosts provide a textbook example of coevolution, by reciprocally selecting for better parasitic tricks (to fool hosts into rearing cuckoo offspring) or better host defences (to avoid rearing a cuckoo chick). However, we know much less about how these arms races between species interact with the social selection pressures within species.

The weavers (Ploceidae) provide a unique opportunity to investigate such questions. These small birds produce conspicuous, enclosed nests that vary both across and within species. The males produce the nests and the females choose their preferred nests in which to lay eggs. Weavers are also host species of the brood parasitic Diederik cuckoo (Chrysococcyx caprius) and the architectural design of weaver nests is thought to be an important barrier in keeping the cuckoo out of the nest, but we have a surprisingly limited understanding of this fascinating evolutionary interaction.

This project had two main objectives:
(1) Uncover evolutionary mechanisms that explain weaver nest structure: (a) is weaver nest architecture a defence against brood parasitism and if so, how do nests repel cuckoos? (b) to characterise the extent to which female preference for nest characteristics interacts with nest defences against cuckoos; (c) to document and examine the effects of variation in nest defences on host egg patterning (information used by hosts when making decisions about egg rejection), since nest structure influences the light environment in which host and cuckoo eggs are observed by the host.
(2) To draw inspiration from natural structures using interdisciplinary approaches that could provide bio-inspired solutions to problems faced by humans.

Unfortunately, work towards each of these outputs was severely curtailed owing to enduring direct and indirect effects of the global covid pandemic.

Nevertheless some progress was achieved.The project grew from two strands of previous work by the the Researcher, and these continued to provide background detail to the project supported by the Marie Curie Fellowship. One previous strand examined how the appearance of a brood parasite contributes to provoking defences against parasitism by the host. The second strand of work investigated the breeding biology of weaverbirds. Even though it proved impossible to reach any conclusions about the two main objectives of the current project, five papers / preprints were produced in relation to these preliminary strands of work.
The Researcher established field sites, logistics and local networks for examining the nest architecture of weavers and their interactions with Diederik cuckoo brood parasites. Initial field data was collected and analysed (see below for more details), including physical nest morphometrics, and data were extracted from calibrated and reliable imaging approaches. The Researcher also had online meetings with named collaborator Prof Stoddard in Princeton. Although the initial results of this work were suggestive of relationships existing between different nest characteristics measured from an individual nest, and between nest characteristics and the social environment, it was not possible to analyse the data further or to collect more data to follow up these promising lines of enquiry.

Before starting work on investigating the role of nest characteristics in contributing to defences against cuckoos, it was necessary for the Researcher to use the first year of work to conduct some preliminary investigations into the other factors that contribute to host defences against cuckoos. Part of this work was an invited review considering the adaptive value of cuckoo resemblance to hawks, the physiological responses it evokes in hosts and therefore the type of defences that are then mounted (York 2021, Frontiers in Ecology and Evolution).

A second part of this work involved some field experiments conducted in South Africa between October 2019 and March 2020 on diederik cuckoos their host, the southern red bishop. The sexes differ in Diederik cuckoos, with females bearing duller plumage than males and sporting a brown iris and eye-ring rather than the crimson equivalents displayed by the males. The experiments revealed that hosts were just as likely to mob a male cuckoo or a female cuckoo (or a control). Curiously, though, the incidence of egg-rejection was greater when a male cuckoo visited the nest than when a female cuckoo visited. The results suggest that, independent of any nest characteristics, the female's drabber appearance might be adaptive in eliciting weaker rejection defences by hosts than is seen in response to males (York 2024, Ecology and Evolution).

Meanwhile, background work on the breeding biology of weavers was brought fruition through the publication of three preprints/ papers. The first investigated the role of prolactin in regulating parental care and helping behaviour in white-browed sparrow weavers (Walker et al 2021 BioRxiv). The second considered how rainfall and social dominance contribute to telomere dynamics (Wood et al 2022 Molecular Ecology). The third paper examined the trade-off that exists between helping behaviour and dispersal in males and females (Capilla-Lasheras et al. 2024 PLoS Biology).
One technical aim of this project was to develop non-destructive methods for monitoring active nests in the field to: (1) generate highly quantitative data on nest characteristics that are (2) repeatable, reproducible and sustainable, (3) reduce disturbance to active nests in the wild, partly through collaboration with Prof Stoddard at the University of Princeton. Although initial steps towards developing these methods were successful, it was not possible to complete the work that was planned originally owing to the enduring effects of the covid pandemic.

A second goal was to use the project to provide opportunities for education and training via research for undergraduate and graduate students, with direct benefits for the students in terms of skill development, and for society in terms of disseminating the scientific approach through research-led teaching. A master's student and undergraduate project students were recruited to this end, with local support from the host institution - but supervision of their projects could not be undertaken by the Researcher, for the reasons given above. The projects were taken over by alternative supervisors but had to be tilted differently to reflect the research skills of the substitute supervisors.

A third goal was to engage a wider public with the results of the research, and this was more successful. The Researcher participated in and led a number of outreach initiatives for local Bird Clubs, Ornithological Societies, and community-facing groups, including a crafting outreach event making decorative bird nests in collaboration with the Women’s Institute and Cambridge Museum of Zoology.
southern masked weaver Ploceus velatus with nest
lesser masked weaver Ploceus intermedius with nest
weaver nest non-destructive imaging methodology
southern red bishop Euplectes orix nest
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