Machine learning reveals cryptic dialects that guide mate choice in a songbird

Abstract

Culturally transmitted communication signals, such as human language or bird song, can change over time through a process of cultural drift, and may consequently enhance the separation of populations, potentially leading to reproductive isolation. Local song dialects have been identified in bird species with relatively simple songs where individuals show high cultural conformity. In contrast, the emergence of cultural dialects has been regarded as unlikely for species with more variable song, such as the zebra finch (Taeniopygia guttata). Instead, it has been proposed that selection for individual recognition and distinctiveness may lead to a complete spread across the space of acoustic and syntactical possibilities. However, another possibility is that analytical limitations have meant that subtle but possibly salient group differences have not yet been discovered in such species. Here we show that machine learning can distinguish the songs from multiple captive zebra finch populations with remarkable precision, and that these cryptic song dialects drive strong assortative mating in this species. We studied mating patterns across three consecutive generations using captive populations that have evolved in isolation for about 100 generations. Cross-fostering eggs within and between these populations and quantifying social interactions of the resulting offspring later in life revealed that mate choice primarily targets cultural traits that are transmitted during a short developmental time window. Detailed social networks showed that females preferentially approached males whose song resembled that of their adolescent peers. Our study shows that birds can be surprisingly sensitive to cultural traits for mating that have hitherto remained cryptic, even in this well-studied species that is used as a model for song-learning.

Broad‐scale applications of the Raspberry Pi: A review and guide for biologists

“…(2018) and Wang et al. (2021) used multiple Raspberry Pi's as part of a long‐term, automated recording and monitoring system of groups of birds in outdoor aviaries. Finally, Heuschele et al.…”

Generalisation of early learned tutor song preferences in female zebra finches (Taeniopygia guttata)

“…Albeit that the songs of these birds shared significantly more elements with the tutor (father) than unfamiliar control songs (unfamiliar brothers' songs: 53% ± 10%; unfamiliar songs: 19% ± 11%), they were not preferred. This is surprising given that other studies in the zebra finch reported preferences for (foster) brothers' songs and peer group songs (Holveck and Riebel, 2010;Honarmand et al, 2015) or microdialects (Wang et al, 2022). However, sample sizes in Riebel and Smallegange (2003) were small overall (18 birds from only four families) so that the different learning outcomes in tutees from different tutors (Tchernichovski et al, 2021) could have had an unduly influence.…”

Fitness costs of female choosiness are low in a socially monogamous songbird

“…The 4 populations have been maintained in separate aviaries (without visual and with limited auditory contact). When birds from 2 different populations (combining S with B and K with M) were brought together in the same breeding aviary, they formed social pairs that were predominantly assortative with regard to population (87% assortative pairs), despite the fact that opposite-sex individuals were unfamiliar with each other ([ 52 ]; see also [ 62 ]). To find out whether this assortative mating took place because of genetic (e.g., body size) or cultural (e.g., song) differences, we produced an offspring generation (“F1”) in which half of the birds were cross-fostered between populations (between S and B or between K and M) and half of the birds were cross-fostered within populations.…”

“…One practical obstacle is that the costs of choosiness can only be measured if one finds a sufficiently strong preference that will be reliably expressed by the choosing sex. In zebra finches, a socially monogamous bird that forms lifelong pair bonds, females reliably prefer (unfamiliar) males that have learned their song in the same population in which females grew up, over males with song from a different population [ 52 ]. Working with 4 independent captive populations (2 domesticated and 2 recently wild derived), we used cross-fostering of eggs between populations to produce 2 different cultural lineages (A and B) within each population that differ only in their song dialects.…”

“…The lineages were bred in isolation for one additional generation, to obtain birds from the same genetic population that differ only in the song that the foster grandparents once transmitted to the parents of the current generation. When bringing together equal numbers of unfamiliar males and females of the 2 song dialects A and B, on average, 73% of pairs formed assortatively by dialect (random expectation: 50% [ 52 ]). We made use of this moderately strong assortative mating preference to design an experimental study with preregistered methods of data collection and analysis plan ( https://osf.io/8md3h ), ensuring maximal objectivity in the quantification of fitness costs of choosiness.…”