The evolution of extended phenotypes and associated signals in animals : weaverbirds’ nests and sexual selection as a case study – EXTENDEDPHENOTYPE

Objective 1 – Diversification of nest architecture in the weaver’s family and associated visual and vocal signals. We started by determining the ecological, life-history and socio-sexual factors associated with the diversity of nest architecture (Work Package 1). We will then study the association between nests characteristics, and sexual ornaments such as visual and acoustic displays (Work Package 2). For this, we will use modern phylogenetic comparative methods (PCM’s), and rely on a recent phylogeny of the Ploceidae. If some aspects of nest architecture (size, shape, material) have a sexually selected signalling function, we expect them to be (i) more elaborated in species under stronger sexual selection, (ii) positively associated with sexual displays that are independent targets of sexual selection or that advertise the nest, and (iii) negatively associated with costly displays or signals through allocation trade-offs.
Objective 2 – Evolution of nest building behaviour and associated visual and vocal signals in the sociable weaver. To determine if nest building behaviour can be in itself a secondary sexual signal, we conduct detailed observational and experimental work at the level of one species, the sociable weaver. Chosing this species will allow us to work on an established population that we have monitored since 2010, with individually marked birds and known histories, and hence to fitness measures. The sociable weaver is a colonial species that builds communally a nest mass weighing up to one ton (Fig 1). In Work Package 1, we use observations and modern technologies based on radio-frequency identification (RFID), artificial intelligence (deep learning) and image analyses to determine how nest building activity varies along the season, who builds more, where and how, and how conspicuous nest building is. In Work Package 2, we will use observational and experimental approaches to investigate whether nest building is a sexually selected signal, i.e. whether it is sensitive to male-male competition and female audience. Finally, in Work Package 3, we will measure the links between nest building, mate choice and fitness in order to assess the potential of sexual selection to promote the evolution of nest building.

We started by determining the ecological, life-history and socio-sexual factors associated with the diversity of nest architecture (Work Package-(WP) 1). For this, we build a data base containing all the known reproductive, social and morphological information available in the literature on the weaver family. In addition, photos of 1296 nests and 62 species have been obtained either for the British natural history museum (online collection), Phown data base and from a field expedition conducted in January 21.

We worked on WP2 which aims to study the association between nest characteristics and sexual ornaments such as visual and acoustic displays. We went to the field in January 21. We managed to collect song and display on about 18-20 species in on month of fieldwork (4 persons in the field). We had a meeting with Fanny Rybak in June 2021 to determine the acoustic analyses to be performed.

In Objective 2, we work at the level of one species, the sociable weaver. We aim to determine if nest building behaviour can in itself be a secondary sexual signal. To complete this objective, one PhD student was engaged at cefe in October 2021: Nicolas Silva.
The aim is of our WP1 is to determine who builds more, where and how, and how conspicuous nest building is. To this aim we captured and equipped birds of 15 colonies with colour rings. Several trained field assistants made behavioural observations. We have 720 hours of observations, corresponding to 3382 building events with information about the individual, the location of the building and the nest material used, and more than 2000 building events without any information on the event. These data should be analysed in 2021/22. We in addition attached a pit at the ring of the birds at 6 colonies and positioned camera to film the building events. Building videos data are collected since February 2021. We collected about 2000 hours of videos on 3 colonies. Raspberry PI and camera associated to RFID stations automatically collected photos of the back of the birds coming at the feeders to have their ID (Ferreira et al. 2020, Method in Ecol. Evol).

In parallel, we develop the use of AI in this project. N. Silva (CEFE) implemented the use of mask RCNN (IA) to automatically measured the size of the black bib of the birds based on photos and implemented automatic detection of birds on videos. . Last the funding we obtained through this ANR allows to enrich and exploit the long term data set and this work led to the publications of one paper in Ecol. Letter (d’Amelio et al. in press.) and one submit to J. of Anim Ecol questioning the mating system of our study species (d’Amelio et al. in prep.)

For objective 1, the next steps is to run Bayesian phylogenetic generalised linear mixed models (PGLMM) and to go back to the field

For objective 2, the next major step is to identify the builders based on a combination of technologies relying on radio-frequency identification (RFID), image analyses of building videos, and artificial intelligence (deep learning).

D'Amelio, P.; Ferreira, A.; Fortuna, R.; Paquet, M.; Silva, L. ; Theron, F.; Doutrelant, C.; Covas, R. In press. Disentangling climatic and nest predator impact on reproductive output reveals adverse high temperature effects regardless of helper number in an arid-region cooperative bird Ecology Letter

Extended phenotypes are traits produced outside the body of the individual which carries the genes coding for their expression. Spider webs, decorated structures constructed by bower birds, animal nests or human houses are all well-known examples of these taxonomically widespread traits. However, almost four decades after Dawkins’ first introduction of this concept, the evolutionary mechanisms accounting for the striking diversity of extended phenotypes remain poorly understood.

While the evolution of many extended phenotypes may have initially been favoured by their protective function, many appear also to serve as sexual signals. Hence, sexual selection may explain not only the evolution of bright colours, elaborate songs and dances, but also of attractive structures that are not part of an organism body. Studies on a wider array of species are needed to determine the importance of sexual selection in the diversification of extended phenotypes, and also to understand how extended phenotypes relate to other signals of the same animals. Specifically, since extended phenotypes are traits dissociated from the body, they should co-evolve with other signals indicating the identity and/or quality of the owners, but this prediction remains to be tested.

We propose to work on one of the most spectacular and diverse radiations of extended phenotypes, the intricate and complex nest architectures of weaverbirds (117 species). Our aim is to investigate, in particular, the role of sexual selection in the evolution and diversification of (i) nest architecture (Objective 1) and (ii) nest building behaviour (a potential display associated with the extended phenotype; Objective 2). For both traits, we also aim to determine how they relate to the other ‘classic’ ornaments – striking colours, songs, and/or flight displays.

In Objective 1, we will work at the interspecific level. We will start - Work Package-(WP) 1- by determining the ecological, life-history and socio-sexual factors associated with the diversity of nest architecture. In WP2, we will study the association between nest characteristics, and sexual ornaments such as visual and acoustic displays. In Objective 2, to determine if nest building behaviour can in itself be a secondary sexual signal, we will conduct detailed observational and experimental work at the level of one species, the sociable weaver. Working on this species will give us access to an established population that we have monitored since 2010, and hence to individually marked birds with known histories, including fitness measures. We will use modern technologies based on radio-frequency identification (RFID), image analyses and artificial intelligence (deep learning) to determine who builds more, where and how, and how conspicuous nest building is (WP1). We will test experimentally the prediction that if nest building is a sexually selected signal in males, it should be sensitive to male-male competition and to female audience (WP2). Finally, to assess the potential of sexual selection to promote the evolution of nest building, we will measure the links between nest building, female preference, and fitness (WP3).

The feasibility and impact of our project is ensured by the expertise of the whole team in the fields of sexual selection, visual and acoustic communication, as well as our experience with the study models and the methods used (e.g. comparative analyses). In addition, the use of ground-breaking techniques, such as Artificial Intelligence, RFID technology and on board microphones will allow us to obtain a large volume of high quality data that will markedly increase the profile and impact of our results. Our results will be disseminated through conferences, university courses, social networks, and collaborations with artists.