Like Father Like Son: Cultural and Genetic Contributions to Song Inheritance in an Estrildid Finch

Social learning of vocalizations is integral to song inheritance in oscine passerines. However, other factors, such as genetic inheritance and the developmental environment, can also influence song phenotype. The relative contributions of these factors can have a strong influence on song evolution and may affect important evolutionary processes such as speciation. However, relative contributions are well-described only for a few species and are likely to vary with taxonomy. Using archived song data, we examined patterns of song inheritance in a domestic population of Java sparrows (Lonchura oryzivora), some of which had been cross-fostered. Six-hundred and seventy-six songs from 73 birds were segmented and classified into notes and note subtypes (N = 22,972), for which a range of acoustic features were measured. Overall, we found strong evidence for cultural inheritance of song structure and of the acoustic characteristics of notes; sons’ song syntax and note composition were similar to that of their social fathers and were not influenced by genetic relatedness. For vocal consistency of note subtypes, a measure of vocal performance, there was no apparent evidence of social or genetic inheritance, but both age and developmental environment influenced consistency. These findings suggest that high learning fidelity of song material, i.e., song structure and note characteristics, could allow novel variants to be preserved and accumulate over generations, with implications for evolution and conservation. However, differences in vocal performance do not show strong links to cultural inheritance, instead potentially serving as condition dependent signals

Like Father Like Son: Cultural and Genetic Contributions to Song Inheritance in an Estrildid Finch

From Frontiers via Jisc Publications RouterHistory: collection 2021, received 2021-01-15, accepted 2021-05-05, epub 2021-06-04Publication status: PublishedSocial learning of vocalizations is integral to song inheritance in oscine passerines. However, other factors, such as genetic inheritance and the developmental environment, can also influence song phenotype. The relative contributions of these factors can have a strong influence on song evolution and may affect important evolutionary processes such as speciation. However, relative contributions are well-described only for a few species and are likely to vary with taxonomy. Using archived song data, we examined patterns of song inheritance in a domestic population of Java sparrows (Lonchura oryzivora), some of which had been cross-fostered. Six-hundred and seventy-six songs from 73 birds were segmented and classified into notes and note subtypes (N = 22,972), for which a range of acoustic features were measured. Overall, we found strong evidence for cultural inheritance of song structure and of the acoustic characteristics of notes; sons’ song syntax and note composition were similar to that of their social fathers and were not influenced by genetic relatedness. For vocal consistency of note subtypes, a measure of vocal performance, there was no apparent evidence of social or genetic inheritance, but both age and developmental environment influenced consistency. These findings suggest that high learning fidelity of song material, i.e., song structure and note characteristics, could allow novel variants to be preserved and accumulate over generations, with implications for evolution and conservation. However, differences in vocal performance do not show strong links to cultural inheritance, instead potentially serving as condition dependent signals

Inheritance of temporal song features in Java sparrows

The inheritance of structural characteristics and individual note parameters is often studied in oscine passerines. However, other song features, such as the temporal characteristics of song, are less well studied. Inheritance of these features could be influenced by a range of factors, including social inheritance, mechanical constraints, genetic relatedness and the developmental environment. Using archived song data, we examined patterns of inheritance of temporal song features, relating to song duration, song tempo and internote intervals, in a laboratory population of Java sparrows, Padda oryzivora, some of which had been cross fostered. Overall, we found strong evidence for cultural inheritance of temporal song features, that is, temporal song features were learned from the social father. We found that song duration was, at most, weakly socially inherited and constrained by a correlation between song tempo and number of notes. Internote gap durations were also influenced by other song features, in particular the duration of the preceding and following notes, although social learning was still apparent when controlling for these features. Across all measures, we found no evidence that temporal song features were affected by genetic relatedness or the developmental environment. Our findings, and those in other species, suggest that temporal song features are likely to be inherited through a combination of the learning of song structure and spectral structure of notes, and specific learning of temporal song features during development

Vocalization can mediate male-male sexual interactions in Java sparrows

Same-sex sexual behaviors do not have direct fitness outcomes, but might be adaptive. This issue is often discussed in group-living animals, where social bonding is crucial. In our captive environment, around 33% of the Java-sparrow (Lonchura oryzivora) males kept in unisex cages have stable bonded partners. Those bonded males often perch side by side and show allopreening and joint-defensive behaviors towards others. In this study, we aimed to determine how males including such same-sex bonded individuals communicate with each other via vocalizations. We introduced same-sex pairs of Java sparrows, which were bonded or non-bonded, in sound-attenuated boxes and compared their recorded vocalizations with those from male-female pairs. For the male-male pairs, we identified two vocalizations that are usually exchanged between paired partners in intimate contexts: mating trills - which are usually emitted by females during successful copulation - and meowing calls - which are given when both members of the pair are in the nest at the same time. We found that males gave mating trills when their partner males were singing courtship songs, or performed trill duets, which sometimes also included meowing calls. Acoustic analyses revealed that there was no difference between male-male and male-female vocalizations. Meowing calls showed greater within-individual variation in duration and other acoustic parameters, but were similar in same-sex and mixed-sex contexts. Our results indicate that male-male pairs exchanged intimate vocal communications just like male-female couples

Potential role of sensory bias in plumage pattern evolution : termite-eating and polka-dots in estrildid finches

Conspicuous colour patterns of animals, such as dots or stripes, can function as sexual and/or social signals. Their evolution is often explained by honest indicator mechanisms or the sensory exploitation hypothesis. In birds, however, the latter scenario has been scarcely tested. According to the sensory exploitation hypothesis, prey-like colour patterns can evolve when they contribute to attracting opposite-sex conspecifics by hitchhiking pre-existing sensory systems (sensory bias) that help foraging. Even without cheating scenarios, visual systems can serve as an underlying factor that facilitates the evolution of both foraging behaviours and colour patterns on the body. To test this idea, we examined the relationship between bird plumage patterns and diet using phylogenetic comparative approaches. Specifically, we focused on white polka-dot plumage patterns in estrildid finches and tested whether such patterns evolved for visual sensory systems that help foraging termites and other gregarious whitish small round prey items. Although we predicted that white polka-dots exist in termite-eater species, and that termite-eating evolved before the white polka-dot pattern, ancestral reconstruction did not reveal clear ancestral states for termite-eating. However, the phylogenetic regression model showed that species with conspicuous white polka-dots tended to be termite-eaters. We also found that estrildids with white polka-dots were likely to become termite-eaters, while those without white polka-dots were likely to become non-termite eaters, according to evolutionary transition analysis. These results are in contrast to the prediction of sensory exploitation hypothesis, wherein diet is believed to trigger the evolution of plumage patterns. However, the results presented here suggest that pre-existing sensory bias for white dots may have promoted the evolution of both termite-eating and white polka-dot plumage patterns in estrildids

Mating success follows duet dancing in the Java sparrow

Mutual interactions between sexes have multiple signalling functions. Duet singing in songbirds is related to mutual mate guarding, joint resource defence, and signalling commitment. Coordinated visual displays of mating pairs are thought to perform similar functions, but are less well understood. The current study evaluated mutual interactions in an Estrildid species to explore the relative importance of duet dancing and male singing in mating success of pairs in a first encounter. When Java sparrows (Lonchura oryzivora) court prospective mates, only males sing. However, both males and females perform courtship dances, often in a duet-like manner. These dances are typically terminated by female copulation solicitation displays (CSDs). In the current study, we observed higher mating success when courtship dances were mutually exchanged, and when males sang. However, the sex initiating the courtship did not affect mating success. Most females produced CSDs after duet dancing but before hearing the entire song, indicating that duet dancing played a crucial role in mating. This finding highlights an unexplored aspect of duetting behaviour in the process of mutual mate choice. These results conflict with the majority of past songbird research, which has interpreted songs as primary behavioural sexual signals

Age-dependent song changes in a closed-ended vocal learner: elevation of song performance after song crystallization

Birdsong is a sexual signal that serves as an indicator of male quality. There is already abundant evidence that song elaboration reflects early life-history because early developmental stress affects neural development of song control systems, and leaves irreversible adverse effects on song phenotypes. Especially in closed-ended vocal learners, song features crystallized early in life are less subject to changes in adulthood. This is why less attention has been paid to lifelong song changes in closed-ended learners. However, in the eyes of female birds that gain benefits from choosing mates based on male songs, not only past but also current conditions encoded in songs would be meaningful, given that even crystallized songs in closed-ended learners would not be identical in the long term. In this study, we examine within-individual song changes in the Java sparrow Lonchura oryzivora, with the aim of shedding light on the relationship between song and long-term life history. Specifically, we compared song length, tempo, and song complexity measures between the point just after song crystallization and around 1 yr later, and also compared those traits between fathers and sons to clarify the effect of vocal learning. While it is not surprising that song complexity did not differ depending on age or between fathers and sons, we found that song length and tempo increased with age. Follow-up analyses have revealed that frequency bandwidth and peak frequency of song notes also elevated with age. Our results show that song performance related to motor skills can be improved even after song crystallization. We also suggest that song performance in closed-ended vocal learners gives a reliable clue for mate choice by reflecting male quality with aging

Evolution of courtship display in Estrildid finches: dance in relation to female song and plumage ornamentation

Estrildid finches are known for great interspecific diversity in the degree of elaboration in courtship dance, song and plumage coloration and also for the considerable sex differences in these traits within species. To study the evolution of multimodal sexual signaling in these taxa, we collected data on 85 species and analyzed them in a phylogenetic comparative study. As dances are often displayed in parallel with songs and include behavioral elements to emphasize coloration, they are likely to evolve non-independently of songs and plumage characteristics. Hence, we hypothesized that the degree of elaboration in dance would be associated with song and plumage ornamentation due to correlated responses between traits. Alternatively, each sexual signal may evolve independently of the others under the influence of different aspects of reproductive ecology or life history. Finally, because trait expression occurs in both males and females and can be caused by pleiotropic effects, we predicted correlated exaggerations of the traits between sexes as well. We found that courtship dance, song and plumage coloration evolve independently, as these traits were not correlated among species in either sex (i.e., the presence of female song was not related to female dance repertoire). However, we found evidence for correlated responses between the sexes, as species that have males with complex dances or colorful plumage also have females with exaggerated traits. Yet, selection factors acting on these traits were only partially shared between sexes. While coloration can be predicted by intraspecific brood parasitism and dance by body size in females, we were unable to reveal similar relationships in males. Our results indicate that different secondary sexual characters in Estrildid finches evolved under the influence of complicated selection factors, in which both correlated responses between sexes as well as independent selective mechanisms play roles.During this study, Masayo Soma received a JSPS Grant-in-Aid for Young Scientists (23680027), while László Z. Garamszegi was supported by funds from the Spanish government within the frame of the “Plan Nacional” program (ref. no. CGL2012-38262, CGL2012-40026-C02-01).Peer reviewedPeer Reviewe

Evolution of patterned plumage as a sexual signal estrildid finches

Color patterns, such as bars or dots that cover the body surface of animals are generally thought to play roles in signaling and camouflage. In birds, however, the macroscopic aspects of plumage coloration are less well understood, as past studies typically described plumage colorations by using spectrophotometric analyses. To provide insight into the evolution of plumage patterns as sexual signals, we characterized interspecific and intersexual variations in the plumage patterns of estrildid finches and tested their associations with other courtship signals and life-history traits using a comparative phylogenetic approach. Our results support the idea that plumage patterns in estrildids are favored by sexual selection because large-sized conspicuous plumage patterns are possessed by species with an elaborate courtship dance. These plumage patterns may also play roles in social signaling because patterns are more conspicuous in species with intraspecific brood parasitism. We predict that pattern traits can be favored by mate choice or intrasexual competition when they can serve as honest indicators of individual condition. As our results are consistent between the sexes, we suggest that the same selective force is acting on the evolution of plumage patterns in males and females in parallel. Finally, we also found a trade-off between large size and vivid color patterns, suggesting that too conspicuous patterns are costly, presumably because of the risk of catching the eyes of potential predators. Therefore, plumage patterns are also shaped by natural selection