Learned vocal variation is associated with abrupt cryptic genetic change in a parrot species complex

Abstract

Contact zones between subspecies or closely related species offer valuable insights into speciation processes. A typical feature of such zones is the presence of clinal variation in multiple traits. The nature of these traits and the concordance among clines are expected to influence whether and how quickly speciation will proceed. Learned signals, such as vocalizations in species having vocal learning (e.g. humans, many birds, bats and cetaceans), can exhibit rapid change and may accelerate reproductive isolation between populations. Therefore, particularly strong concordance among clines in learned signals and population genetic structure may be expected, even among continuous populations in the early stages of speciation. However, empirical evidence for this pattern is often limited because differences in vocalisations between populations are driven by habitat differences or have evolved in allopatry. We tested for this pattern in a unique system where we may be able to separate effects of habitat and evolutionary history. We studied geographic variation in the vocalizations of the crimson rosella (Platycercus elegans) parrot species complex. Parrots are well known for their life-long vocal learning and cognitive abilities. We analysed contact calls across a ca 1300 km transect encompassing populations that differed in neutral genetic markers and plumage colour. We found steep clinal changes in two acoustic variables (fundamental frequency and peak frequency position). The positions of the two clines in vocal traits were concordant with a steep cline in microsatellite-based genetic variation, but were discordant with the steep clines in mtDNA, plumage and habitat. Our study provides new evidence that vocal variation, in a species with vocal learning, can coincide with areas of restricted gene flow across geographically continuous populations. Our results suggest that traits that evolve culturally can be strongly associated with reduced gene flow between populations, and therefore may promote speciation, even in the absence of other barriers.

Figure 1. Overview of study sites and contact call variation.

(a) Distribution of Platycercus elegans (grey overlay) showing recording sites. The yellow squares are recording sites with yellow phenotype birds; red squares are recording sites with crimson phenotype birds. The dots inside the squares indicate the mtDNA of the population: yellow dots = yellow subspecies (P. e. flaveolus), purple spots = hybrid Western Slopes population, red dots = crimson subspecies (P. e. elegans). The cut out gives a more detailed look of the six recording sites where the clines in microsatellite markers occur. The blue line denotes the Murray-Murrumbidgee river system. (b) Spectrogram with waveform of two contact calls from Berri (in the P. e. flaveolus distribution). (c) Spectrogram with waveform of a contact call from the clinal microsatellite area. (d) Spectrogram with waveform of two contact calls from Brungle (in the hybrid Western Slopes population).

Figure 2. Plots of the microsatellite population assignment (using STRUCTURE) and all five acoustic variables clines.

Dots are the mean values for each individual. The three plumage forms/subspecies are indicated by dot colour as follows: P. e. flaveolus, yellow dots; the Western Slopes population, purple dots; P. e. elegans, red dots. Green lines connect the means of each population, and the dotted line within the vocalization plots indicates the microsatellite cline for comparison. At this latitude 1 degree of longitude is roughly 92km, and the transect changes little with latitude (Fig. 1).

Figure 3. Results from a Mantel test analyzing the relationship between vocal variation (Euclidean distances based on the five acoustic variables between all the recording sites) and geographic distances between recording sites (R² = 0.143; p = 0.036).