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

We collected nest photos, taken in natural history museums and in the field. We measured the scale invariance of the nests and of the habitats. We used bayesian phylogenetic comparative methods , and relied on a recent phylogeny of the Ploceidae. We investigated the potential role of sexual selection in shaping nest visual patterns of 61 species, focusing on scale-invariance, a property describing how patterns remain visually similar across spatial scales. We collected acoustic data on xeno canto and in the field and determine how mating sytem and sociality affect acoustic diversity. We run a metaanayse to determine to which extent acoustic diversity is positively impacted by sexual selection in birds.

To determine if nest building behaviour can be in itself a secondary sexual signal, we conducted detailed observations during fours years and performed experimental work at the level of one species, the sociable weaver. The sociable weaver is a colonial species that builds communally a nest mass weighing up to one ton. We used 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 and who builds more. We also conduced behavioural tests to examine materiel preference in both sexes. In parallel, we run long term data base analyses to describe mating system, sociality and dominance in this species . We implemented AI in the field and to speed up video analyses.

Objective 1. We found that weaver nest patterns are more similar to those of the environment when nests are more likely to be under sexual selection (i.e. when species are polygynous and sexually dimorphic, their nests match the scale invariance of natural habitats more closely). However, with respect to vocal patterns, we found that polygynous species produce less diverse songs, suggesting that sociality rather than sexual selection drives song diversity. Last our meta-analysis showed that the effect of sexual selection on song diversity observed in weaver birds is opposite to what is reported in other species.

Objective 2. Analyses of 14,000 nest-building events show that sociable weavers maintain their communal canopy throughout the year, investing substantial time and effort in its construction and maintenance. Males are 8 times more likely to build the common and build more intensively than females with longer straws. Breeders build more than helpers and males helpers build more than females helpers, both breeders and helpers build more when they have no chick to rear. Long-term data show that this species exhibits lifelong monogamy, with pairs remaining together for life. Dominance increases with age, and individuals with more social connections (friends) show greater longevity.

We also developed a Raspberry Pi–based camera system connected to RFID stations, allowing the automatic collection of photographs of the backs of birds visiting feeders. We found that AI-based identification outperformed human observers. In parallel, we expanded the use of AI in this project by implementing Mask R-CNN to automatically measure the size of birds’ black bibs from photographs and determine their sex. We also implemented automatic detection of birds and their behaviours in video recordings

Oustanding feature:

Nest architecture functions as an extended phenotype shaped by sexual selection through fine-scale matching with environmental structure.

Long-term behavioural data uncovers the central role of age in dominance, shows all contribute to the common but males do it more and link social connectivity and survival. The study also provides rare empirical evidence of lifelong monogamy in a highly social avian species. Finally, the integration of AI-based monitoring enables unprecedented individual-level resolution, surpassing human identification and opening new avenues for large-scale behavioural ecology.

Future prospects:

This project opens numerous avenues for future research, both in field-based studies and from a comparative perspective.

At the comparative level, future work could (i) focus on nest architecture, particularly nest shape, in relation to sexual selection. (ii) It could involve establishing collaborations with theoretical modellers to develop robust evolutionary frameworks and generate clear predictions regarding potential trade-offs and correlations among song characteristics, plumage coloration, and the presence or absence of extended phenotypes. (iii) The methods developed in this ANR should also be applied to other species to assess the extent to which visual patterns derived from extended phenotypes may be subject to sexual selection across taxa.

In sociable weavers, future research should aim to (i) determine whether nest-building behaviour is repeatable over time and whether it is correlated with other cooperative behaviours. This will allow us to test for the existence of consistent individual differences (i.e. personalities), with some individuals contributing more to collective activities than others. (ii) Further development of AI-based approaches will be essential to more precisely identify when and how individuals—particularly males—contribute to the common good, and to uncover the mechanisms underlying variation in cooperative investment. (iii) More broadly, more work should deepen our understanding of the interactions among mate choice, sociality, cooperation, and conflict in a cooperative society characterized by reduced reproductive opportunities—a system that, in several respects, parallels key features of human social organization.

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.