Emma I. Greig

Song evolution in Maluridae: influences of natural and sexual selection on acoustic structure

Abstract Many factors may influence the evolution of acoustic signals, including sexual selection, morphological constraints and environmental variation. These factors can play simultaneous and interacting roles in determining signal phenotypes. Here, we assess the evolution of song features in the Maluridae, a passerine family with significant variation among taxa in levels of sperm competition, morphological features and breeding habitats ranging from arid grasslands in Australia to tropical rainforests in New Guinea. We used phylogenetic comparative methods and a robust molecular phylogeny to compare song characteristics with a variety of other measures, including testes mass, body-size and latitude. Several aspects of the temporal and frequency structure of song were associated with relative testes mass, suggesting that sexual selection may influence some song characteristics in this family. The lowest frequencies of song were strongly predicted by body-size, indicating that morphological constraints have also likely influenced acoustic phenotypes. Song versatility, reflecting the diversity of note types in a song, was positively correlated with latitude, suggesting that complexity may increase in association with more temperate or variable environments. Variation in song structure across the family appears to reflect a complex interaction between natural and sexual selection.

Sons learn songs from their social fathers in a cooperatively breeding bird

Song learning is hypothesized to allow social adaptation to a local song neighbourhood. Maintaining social associations is particularly important in cooperative breeders, yet vocal learning in such species has only been assessed in systems where social association was correlated with relatedness. Thus, benefits of vocal learning as a means of maintaining social associations could not be disentangled from benefits of kin recognition. We assessed genetic and cultural contributions to song in a species where social association was not strongly correlated with kinship: the cooperatively breeding, reproductively promiscuous splendid fairy-wren (Malurus splendens). We found that song characters of socially associated father–son pairs were more strongly correlated (and thus songs were more similar) than songs of father–son pairs with a genetic, but no social, association (i.e. cuckolding fathers). Song transmission was, therefore, vertical and cultural, with minimal signatures of kinship. Additionally, song characters were not correlated with several phenotypic indicators of male quality, supporting the idea that there may be a tradeoff between accurate copying of tutors and quality signalling via maximizing song performance, particularly when social and genetic relationships are decoupled. Our results lend support to the hypothesis that song learning facilitates the maintenance of social associations by permitting unrelated individuals to acquire similar signal phenotypes.

Differential rates of phenotypic introgression are associated with male behavioral responses to multiple signals.

Sexual selection on multiple signals may lead to differential rates of signal introgression across hybrid zones if some signals contribute to reproductive isolation but others facilitate gene flow. Competition among males is one powerful form of sexual selection, but male behavioral responses to multiple traits have not been considered in a system where traits have introgressed differentially. Using playbacks, mounts, and a reciprocal experimental design, we tested the hypothesis that male responses to song and plumage in two subspecies of red‐backed fairy‐wren (Malurus melanocephalus) explain patterns of differential signal introgression (song has not introgressed, whereas plumage color has introgressed asymmetrically). We found that males of both subspecies discriminated symmetrically between subspecies’ songs at a long range, but at a close range, we found that aggression was equal for both subspecies’ plumage and songs. Taken together, our results suggest that male behavioral responses hinder the introgression of song, but allow for the observed asymmetrical introgression of plumage. Our results highlight how behavioral responses are a key component of signal evolution when recently divergent taxa come together, and how differential responses to multiple signals may lead to differential signal introgression and novel trait combinations.

The couple that sings together stays together: duetting, aggression and extra-pair paternity in a promiscuous bird species

When individuals mate outside the pair bond, males should employ behaviours such as aggression or vocal displays (e.g. duetting) that help assure paternity of the offspring they care for. We tested whether male paternity was associated with aggression or duetting in the red-backed fairy-wren, a species exhibiting high rates of extra-pair paternity. During simulated territorial intrusions, aggression and duetting were variable among and repeatable within males, suggesting behavioural consistency of individuals. Males with quicker and stronger duet responses were cuckolded less often than males with slower and weaker responses. In contrast, physical aggression was not correlated with male paternity. These results suggest that either acoustic mate guarding or male–female vocal negotiations via duetting lead to increased paternity assurance, whereas physical aggression does not.

The Effects of Sex, Age, and Social Status on Annual Survival in the Splendid Fairy-Wren

Abstract. Survival is a critical life-history trait, and among cooperative breeders survival may be linked to the evolution of social organization. We used multi-state models in the program MARK to estimate apparent survival in the Splendid Fairy-wren (Malurus splendens), a cooperatively breeding species in which most pairs are assisted by male offspring from previous generations. We examined survival as it relates to sex, age, and social status (nestling, auxiliary, breeder), and quantified the probabilities of transition between social states. The best-supported model was one in which survival rates differed by social state, survival of auxiliaries and breeders varied annually in the same manner, and the effect of sex varied annually but influenced the survival rate of each group in the same manner. In both males and females overall survival estimates of auxiliaries were similar to those of breeders, whereas survival estimates of adult males were higher than those of females, although the effect of sex varied annually. The probability of transition between categories of social status varied in a manner expected for a cooperatively breeding species: nestling males were more likely than nestling females to become auxiliaries, whereas females were more likely to become breeders in the subsequent year. Similarly, among auxiliaries, females were more likely than males to become breeders. Survival of males being higher that of females likely contributes to the male-biased sex ratio observed in adults of this species and, indirectly, the propensity of younger males to delay dispersal.

How do novel signals originate? The evolution of fairy-wren songs from predator to display contexts

Revealing the evolutionary origin of novel traits is a long-standing challenge in evolutionary biology. The dynamics of antipredator signalling and conspecific advertisement provide one framework in which to investigate this phenomenon, because shifts in signal context may lead to new signal functions, novel evolutionary pressures and ultimately novel phenotypes. Several species of fairy-wrens (Maluridae: Malurus) give song-like trills (‘Type II song’) in response to vocalizations of avian predators. Despite this predator context, in some species the trills appear to function as conspecific-directed displays. We investigated two hypotheses for the evolutionary origin of predator-elicited Type II songs: (1) they originated as antipredator signals, then shifted to a display context and subsequently became more elaborate because selection pressures changed; or alternatively (2) they originated as conspecific-directed songs, then shifted to a predator context to exploit an effective communication window. Using predator playbacks and samples of natural dawn chorus recordings, we found that many Malurus species gave trills in response to predators, but only a subset gave unprompted trills during dawn chorus displays, and ancestral state reconstructions suggested that the predator-elicited context evolved first. Additionally, species that used trills more often (in both predator and unsolicited contexts) tended to have longer trills with a faster note rate, suggesting that trills have evolved a higher performance as they became a more important part of the display repertoire. Our results support the hypothesis that trill displays originated through the elaboration of predator context calls and provide an example of a shift in signal context leading to novel signal phenotypes.

Risk-based alarm calling in a nonpasserine bird

Recent studies have demonstrated the presence of risk-based variation in alarm calling in many vertebrate species. Most of the studies on birds, however, have focused on passerine systems perhaps due to the traditional view that passerine vocalizations are more complex. We investigated the presence of a risk-based alarm calling system in a nonpasserine, the herring gull, Larus argentatus, by recording birds presented with varying degrees of threat, and experimentally exposing and quantifying responses to manipulated alarm calls. We found that herring gulls communicate threat urgency in their alarm calls using both frequency and time parameters. Sound recordings indicated that herring gulls change centre frequency modulation patterns of their alarm calls, generate frequency discontinuities in notes and increase the rate of calling with increases in perceived threat level. Playback experiments showed that conspecifics pay attention to both frequency and time parameters and respond most urgently to playbacks of high-threat calls at a high call rate. A less urgent response to high-threat calls at a low call rate and to low-threat calls at a high call rate suggests that threat urgency information is reinforced by both call type and call rate in the herring gull system. This study is one of the first demonstrations of a risk-based alarm calling system in a nonpasserine.

Black or red: A sex-linked colour polymorphism in a songbird is maintained by balancing selection

Colour polymorphisms play a key role in sexual selection and speciation, yet the mechanisms that generate and maintain them are not fully understood. Here, we use genomic and transcriptomic tools to identify the precise genetic architecture and evolutionary history of a sex-linked colour polymorphism in the Gouldian finch Erythrura gouldiae that is also accompanied by remarkable differences in behaviour and physiology. We find that differences in colour are associated with an ~72-kbp region of the Z chromosome in a putative regulatory region for follistatin, an antagonist of the TGF-β superfamily genes. The region is highly differentiated between morphs, unlike the rest of the genome, yet we find no evidence that an inversion is involved in maintaining the distinct haplotypes. Coalescent simulations confirm that there is elevated nucleotide diversity and an excess of intermediate frequency alleles at this locus. We conclude that this pleiotropic colour polymorphism is most probably maintained by balancing selection.Colour polymorphisms play a key role in sexual selection and speciation, yet the mechanisms that generate and maintain them are not fully understood. We therefore used genomic and transcriptomic tools to identify the precise genetic architecture and evolutionary history of a sex-linked colour polymorphism in the Gouldian finch Erythrura gouldiae that is also accompanied by remarkable differences in behaviour and physiology. We found that differences in colour are associated with an ~72-kbp region of the Z chromosome in a putative regulatory region for follistatin , an antagonist of the TGF-β superfamily genes. The region is highly differentiated between morphs, unlike the rest of the genome, yet we found no evidence that an inversion is involved in maintaining the distinct haplotypes. Coalescent simulations confirm that that there is elevated nucleotide diversity and an excess of intermediate frequency alleles at this locus. We conclude that this pleiotropic colour polymorphism is most probably maintained by balancing selection.