Raoul F. H. Ribot

Learned Vocal Variation Is Associated with Abrupt Cryptic Genetic Change in a Parrot Species Complex

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.

Does the ring species concept predict vocal variation in the crimson rosella, Platycercus elegans, complex?

Vocal variation may be important in population divergence. We studied geographical variation in contact calls of parrots of the crimson rosella, Platycercus elegans, complex, which is characterized by striking geographical plumage coloration variation. This complex has long been considered a rare example of a ring species (where two divergent forms coexist in sympatry but are connected by a chain of intermediate populations forming a geographical ring). We tested whether contact call variation is consistent with the ring species hypothesis. We recorded calls throughout the ring, including several sites from the three main population groups forming the ring and interfaces between them. We analysed duration, peak frequency, fundamental frequency and frequency modulation. We found significant differences, particularly in fundamental frequency and frequency modulation, at multiple biogeographical scales ranging from local populations to subspecies level. Discriminant function analyses showed some populations could be reliably discriminated from call structure. However, our results provided little support for three key predictions of the ring species hypothesis: (1) calls of the terminal, most divergent forms were not significantly different in three of the four acoustic variables, and differences did not appear to be maintained in sympatry, (2) phenotypically/geographically intermediate populations were not characterized by intermediate calls, and (3) call variation was not concordant with geographical sequence around the ring from one terminal form to the other. Our results underscore the emerging view that the evolutionary histories and phenotypic variability of many long-held ring species may be inadequately described by the ring species hypothesis and require alternative explanations.

Phylogenetic analysis of beak and feather disease virus across a host ring-species complex

Significance The roles of disease and species hybridization in maintaining biodiversity are of wide interest, yet are rarely studied simultaneously in wild populations. Using genomic analysis of beak and feather disease virus in an avian ring-species complex, Platycercus elegans, to our knowledge we find viral phylogenetic structure analogous to Mayr’s ring-species hypothesis for the first time in any pathogen. Across 8 y, the host’s viral prevalence and infection load was lower in hybrid birds and in phenotypically intermediate subspecies. Viral genetic variation did not explain host prevalence or infection load, supporting conclusions that the evolved host response is more important. We show how host–species complexes and viral genomic analyses can provide insight into maintenance of biodiversity. Pathogens have been hypothesized to play a major role in host diversity and speciation. Susceptibility of hybrid hosts to pathogens is thought to be a common phenomenon that could promote host population divergence and subsequently speciation. However, few studies have tested for pathogen infection across animal hybrid zones while testing for codivergence of the pathogens in the hybridizing host complex. Over 8 y, we studied natural infection by a rapidly evolving single-strand DNA virus, beak and feather diseases virus (BFDV), which infects parrots, exploiting a host-ring species complex (Platycercus elegans) in Australia. We found that host subspecies and their hybrids varied strikingly in both BFDV prevalence and load: both hybrid and phenotypically intermediate subspecies had lower prevalence and load compared with parental subspecies, while controlling for host age, sex, longitude and latitude, as well as temporal effects. We sequenced viral isolates throughout the range, which revealed patterns of genomic variation analogous to Mayr’s ring-species hypothesis, to our knowledge for the first time in any host–pathogen system. Viral phylogeny, geographic location, intraspecific host density, and parrot community diversity and composition did not explain the differences in BFDV prevalence or load between subpopulations. Overall, our analyses suggest that functional host responses to infection, or force of infection, differ between subspecies and hybrids. Our findings highlight the role of host hybridization and clines in altering host–pathogen interactions, dynamics that can have important implications for models of speciation with gene flow, and offer insights into how pathogens may adapt to diverging host populations.

Fruitful use of bioacoustic alarm stimuli as a deterrent for Crimson Rosellas (Platycercus elegans)

Abstract Birds cause considerable damage to horticultural crops in Australia each year. The playback of species-specific bioacoustic alarm stimuli has been one of the most promising methods suggested to deal with bird-problems. However, no published studies have tested this method on species of parrots, one of the main avian pests of crops in Australia and globally. Furthermore the effectiveness of this method might be reduced if alarm calls were played back that came from a non-local population. The Crimson Rosella species complex (Platycercus elegans), a parrot with considerable acoustic variation throughout its range, is considered a pest species of several commercial fruit crops. This study tested whether alarm calls from Crimson Rosellas were effective in reducing the activity of Rosellas in apple orchards. Three groups of bioacoustic stimuli were compared: control stimuli, local alarm calls and non-local alarm calls. Our results indicate that the playback of alarm calls from Crimson Rosellas is effective in reducing the activity of Rosellas in orchards over the period of study, and we did not find any difference between the use of local and non-local alarm calls. Our study suggests that playback of alarm calls may be an effective deterrent of rosellas over a broad distribution, at least for short-to medium-term use.

Extreme nomadism in desert waterbirds: flights of the banded stilt

In contrast to well-studied Northern Hemisphere birds with spatially and temporally predictable seasonal migrations, waterbirds in desert biomes face major challenges in exploiting stochastic, rich, yet short-lived resource pulses in vast arid landscapes, leading to the evolution of nomadic behaviour. An extreme example is the banded stilt (Cladorhynchus leucocephalus), an opportunistic colonial breeder at remote inland salt lakes after infrequent rain events. Using satellite telemetry on 21 birds (tracked for a mean of 196.2 days), we reveal extensive, rapid and synchronized movement among individuals to and from salt lakes. Two birds left coastal refugia for the inland following rain, flying 1000–2000 km, while 12 others rapidly moved a mean of 684 km (range 357–1298 km) away from drying inland sites to the coast. Two individuals moved longitudinally across the continent, departing and arriving at the same points, yet travelling very different routes; one bird moving more than 2200 km in less than 2.5 days, the other more than 1500 km in 6 days. Our findings reveal movements nearly twice as long and rapid as recorded in other desert waterbirds. We reveal capability to rapidly detect and exploit ephemeral wetland resource pulses across the stochastic Australian desert.

Proximate cues to phases of movement in a highly dispersive waterfowl, Anas superciliosa

BackgroundWaterfowl can exploit distant ephemeral wetlands in arid environments and provide valuable insights into the response of birds to rapid environmental change, and behavioural flexibility of avian movements. Currently much of our understanding of behavioural flexibility of avian movement comes from studies of migration in seasonally predictable biomes in the northern hemisphere. We used GPS transmitters to track 20 Pacific black duck (Anas superciliosa) in arid central Australia. We exploited La Niña conditions that brought extensive flooding, so allowing a rare opportunity to investigate how weather and other environmental factors predict initiation of long distance movement toward freshly flooded habitats. We employed behavioural change point analysis to identify three phases of movement: sedentary, exploratory and long distance oriented movement. We then used random forest models to determine the ability of meteorological and remote sensed landscape variables to predict initiation of these phases.ResultsWe found that initiation of exploratory movement phases is influenced by fluctuations in local weather conditions and accumulated rainfall in the landscape. Initiation of long distance movement phases was found to be highly individualistic with minor influence from local weather conditions.ConclusionsOur study reveals how individuals utilise local conditions to respond to changes in resource distribution at broad scales. Our findings suggest that individual movement decisions of dispersive birds are informed by the integration of multiple weather cues operating at different temporal and spatial scales.

Intraspecific geographic variation in rod and cone visual pigment sensitivity of a parrot, Platycercus elegans

Variation in wavelength sensitivity among subspecies is unknown among vertebrates. The parrot Platycercus elegans has extreme plumage variation between subspecies ranging from pale yellow to crimson which, with differences in background colour and light environment between subspecies, makes it a good candidate for the evolution of within-species differences in vision. We report differences in visual pigments between populations of P. elegans from two subspecies, providing the first known support for population and subspecies variation in visual pigments within a vertebrate species; it is also the first instance of intraspecific variation in rod sensitivity within any vertebrate species. Differences in wavelength sensitivity of rods and cones corresponded to geographic differences in plumage colour. Between study populations, visual pigments varied but not oil droplets. Adaptive functions for the visual pigment differences are untested but they could cause divergence in behaviours associated with colour as well as in dim light, and provide insights into the role of senses in divergence and speciation.

Host heterozygosity and genotype rarity affect viral dynamics in an avian subspecies complex

Genetic diversity at community, population and individual levels is thought to influence the spread of infectious disease. At the individual level, inbreeding and heterozygosity are associated with increased risk of infection and disease severity. Host genotype rarity may also reduce infection risk if pathogens are co-adapted to common or local hosts, but to date, no studies have investigated the relative importance of genotype rarity and heterozygosity for infection in a wild, sexually reproducing vertebrate. With beak and feather disease virus (BFDV) infection in a wild parrot (Platycercus elegans), we show that both heterozygosity and genotype rarity of individual hosts predicted infection, but in contrasting ways. Heterozygosity was negatively associated with probability of infection, but not with infection load. In contrast, increased host genotype rarity was associated with lower viral load in infected individuals, but did not predict infection probability. These effects were largely consistent across subspecies, but were not evident at the population level. Subspecies and age were also strongly associated with infection. Our study provides novel insights into infection dynamics by quantifying rarity and diversity simultaneously. We elucidate roles that host genetic diversity can play in infection dynamics, with implications for understanding population divergence, intraspecific diversity and conservation.

If waterbirds are nocturnal are we conserving the right habitats

Abstract Waterbirds are key indicators of wetland health and recent declines in their abundance have renewed focus on conservation of their habitats in Australia. Yet conservation efforts have mostly ignored the identification of habitats used at night. In this study we assessed three common species, Grey Teal (Anas gracilis), Chestnut Teal (Anas castanea) and Australian Wood Duck (Chenonetta chubata), during day and night. Thermal imaging technologies were utilised to identify individuals to species, count abundances and observe habitat requirements. We found major differences in abundance between night and day of all three species at our study sites. Further, habitat use of teals differed between nocturnal and diurnal hours, with birds aggregating on the bank during daylight hours and moving onto the water during the night. Our findings suggest that nocturnal waterbird surveys can assist conservation efforts. By monitoring bird numbers by night, the significance of a habitat for feeding and shelter purposes can be determined. Additionally, by studying nocturnal behaviour and habitat use, identification and conservation of important wetlands will be increased.

Pair fidelity in long-lived parrots: genetic and behavioural evidence from the Crimson Rosella (Platycercus elegans)

ABSTRACT Genetic analyses have revolutionised our understanding of avian mating systems. However, the majority of such studies to date have focused on passerine species. Despite this taxonomic bias, extra-pair paternity (EPP) and conspecific brood parasitism (CBP) are usually concluded to be less common in taxa with pronounced longevity, socially monogamous mating systems, and bi-parental care. The order Psittaciformes, with around 350 species worldwide, has long-lived species that are relatively under-studied with respect to parentage and pair fidelity. Although studies have revealed a variety of mating systems in Psittaciformes, there is little work testing whether EPP or CBP occur in Psittaciformes. To test for genetic and social pair fidelity we studied an Australian parrot, the Crimson Rosella (Platycercus elegans), over 8 years at three sites in south-eastern Australia. Using nine microsatellite markers in 42 pairs and their offspring, we found no cases of EPP. However, we found one case of CBP, suggesting that P. elegans females do adopt alternative breeding strategies, albeit at low levels. We also show that over the 8 years of study 32% of recaptured individuals paired with more than one partner in different years. Our results are consistent with assumption of low EPP in parrots, but challenge the notion that this is associated with long-term pair bonds.