Malurus Melanocephalus Research Articles

Testosterone Coordinates Gene Expression Across Different Tissues to Produce Carotenoid-Based Red Ornamentation.

Carotenoid pigments underlie most of the red, orange, and yellow visual signals used in mate choice in vertebrates. However, many of the underlying processes surrounding the production of carotenoid-based traits remain unclear due to the complex nature of carotenoid uptake, metabolism, and deposition across tissues. Here, we leverage the ability to experimentally induce the production of a carotenoid-based red plumage patch in the red-backed fairywren (Malurus melanocephalus), a songbird in which red plumage is an important male sexual signal. We experimentally elevated testosterone in unornamented males lacking red plumage to induce the production of ornamentation and compared gene expression in both the liver and feather follicles between unornamented control males, testosterone-implanted males, and naturally ornamented males. We show that testosterone upregulates the expression of CYP2J19, a gene known to be involved in ketocarotenoid metabolism, and a putative carotenoid processing gene (ELOVL6) in the liver, and also regulates the expression of putative carotenoid transporter genes in red feather follicles on the back, including ABCG1. In black feathers, carotenoid-related genes are downregulated and melanin genes upregulated, but we find that carotenoids are still present in the feathers. This may be due to the activity of the carotenoid-cleaving enzyme BCO2 in black feathers. Our study provides a first working model of a pathway for carotenoid-based trait production in free-living birds, implicates testosterone as a key regulator of carotenoid-associated gene expression, and suggests hormones may coordinate the many processes that underlie the production of these traits across multiple tissues.

Photoperiod and rainfall are associated with seasonal shifts in social structure in a songbird

Abstract Seasonally breeding animals often exhibit different social structures during non-breeding and breeding periods that coincide with seasonal environmental variation and resource abundance. However, we know little about the environmental factors associated with when seasonal shifts in social structure occur. This lack of knowledge contrasts with our well-defined knowledge of the environmental cues that trigger a shift to breeding physiology in seasonally breeding species. Here, we identified some of the main environmental factors associated with seasonal shifts in social structure and initiation of breeding in the red-backed fairywren (Malurus melanocephalus), an Australian songbird. Social network analyses revealed that social groups, which are highly territorial during the breeding season, interact in social “communities” on larger home ranges during the non-breeding season. Encounter rates among non-breeding groups were related to photoperiod and rainfall, with shifting photoperiod and increased rainfall associated with a shift toward territorial breeding social structure characterized by reductions in home range size and fewer encounters among non-breeding social groups. Similarly, onset of breeding was highly seasonal and was also associated with non-breeding season rainfall, with greater rainfall leading to earlier breeding. These findings reveal that for some species, the environmental factors associated with the timing of shifts in social structure across seasonal boundaries can be similar to those that determine timing of breeding. This study increases our understanding of the environmental factors associated with seasonal variation in social structure and how the timing of these shifts may respond to changing climates.

Range shift and loss of genetic diversity under climate change in the red-backed fairywren (Malurus melanocephalus), an Australian endemic bird species

AbstractClimatic variability is the most important force influencing the distribution dynamics of common and widespread species, with significant effects on their current biogeographical patterns. In this study, phylogeography was integrated with ecological niche modelling to understand the range dynamics of an Australian bird species, the red-backed fairywren (Malurus melanocephalus), under various climate change scenarios. Specifically, an ecological niche modelling approach with Bayesian-based phylogeographical analysis was used to develop robust inferences regarding the demographic history of the species. The predictions of the model were mostly consistent with the present distribution of the species. However, under the Last Interglacial bioclimatic conditions, the model predicted a significantly narrower distribution than today, indicating the existence of allopatric refugia. Predictions for the Last Glacial Maximum indicated that the species had a wider distribution, extending northwards. Additionally, predictions for the future (2050 and 2070) indicated that the species will probably have a narrower distribution than at present, which will be shifted eastwards. The extended Bayesian skyline plot analysis, which provides a robust analysis of fluctuations in the effective population size throughout the evolutionary history of a species, produced results highly consistent with the ecological niche modelling predictions for the red-backed fairywren. This is the first study to investigate the Late Quaternary history of an endemic avian taxon from Australia using ecological niche modelling and Bayesian-based demographic analysis.

Sperm Numbers as a Paternity Guard in a Wild Bird.

Sperm competition is thought to impose strong selection on males to produce competitive ejaculates to outcompete rival males under competitive mating conditions. Our understanding of how different sperm traits influence fertilization success, however, remains limited, especially in wild populations. Recent literature highlights the importance of incorporating multiple ejaculate traits and pre-copulatory sexually selected traits in analyses aimed at understanding how selection acts on sperm traits. However, variation in a male’s ability to gain fertilization success may also depend upon a range of social and ecological factors that determine the opportunity for mating events both within and outside of the social pair-bond. Here, we test for an effect of sperm quantity and sperm size on male reproductive success in the red-back fairy-wren (Malurus melanocephalus) while simultaneously accounting for pre-copulatory sexual selection and potential socio-ecological correlates of male mating success. We found that sperm number (i.e., cloacal protuberance volume), but not sperm morphology, was associated with reproductive success in male red-backed fairy-wrens. Most notably, males with large numbers of sperm available for copulation achieved greater within-pair paternity success. Our results suggest that males use large sperm numbers as a defensive strategy to guard within-pair paternity success in a system where there is a high risk of sperm competition and female control of copulation. Finally, our work highlights the importance of accounting for socio-ecological factors that may influence male mating opportunities when examining the role of sperm traits in determining male reproductive success.

Behaviour of probable hybrid Red-backed x Superb Fairy-wrens at Gladstone, Queensland

This note describes observations of the behaviour of two hybrid male fairy-wrens (most likely resulting from crosses between Red-backed Malurus melanocephalus and Superb Fairy-wrens M. cyaneus) at Gladstone, Queensland, and their pairing with two female Red-backed Fairy-wrens.

Social and abiotic factors differentially affect plumage ornamentation of young and old males in an Australian songbird

Both abiotic environmental conditions and variation in social environment are known to impact the acquisition of sexual signals. However, the influences of abiotic environmental and social factors are rarely compared to each other. Here we test the relative importance of these factors in determining whether and when male red-backed fairy-wrens, Malurus melanocephalus , moult into ornamented breeding plumage , a known sexual signal. One-year-old male red-backed fairy-wrens vary in whether or not they acquire ornamentation, whereas males age 2 years and older vary in their timing of ornament acquisition. It is unclear whether these processes are determined by the same or different factors, and we examined both events using a combination of long-term breeding records and nonbreeding social networks. We found that 1-year-old males that paired prior to the start of the breeding season were more likely to acquire ornamented plumage, but rainfall did not influence whether 1-year-old males acquired ornamented plumage. Thus, for young individuals, social cues appear to play a larger role than abiotic environmental factors in determining ornament acquisition. For older males, timing of ornamented plumage acquisition was constrained by rainfall, with drier nonbreeding seasons leading to poorer physiological condition and later moult dates. Thus, sexual signal variation in older males appears to be a condition-dependent trait, driven by abiotic environmental and physiological factors rather than social cues. These findings reveal that factors influencing sexual signal expression can vary with age when age classes exhibit different forms of signal variation. Our results suggest that social environment may drive sexual signal variation in young individuals, whereas abiotic environmental variation may drive sexual signal variation in older individuals. • The factors influencing sexual signal expression remain unclear. • Social factors determined whether 1-year-old males acquired ornamented plumage. • Rainfall determined when older males acquired ornamented plumage. • Factors influencing sexual signal expression can vary with age.

Wildfire affects expression of male sexual plumage through suppressed testosterone circulation in a tropical songbird

Natural disturbances like drought and wildfires are expected to increase in prevalence, so understanding how organisms are affected is a key goal for conservationists and biologists alike. While many studies have illustrated long‐term effects of perturbations on survival and reproduction, little is known of short‐term effects to physiology and sexual signal expression. Ornamental traits have been proposed as reliable indicators of environmental health, yet studies are lacking in the context of natural disturbances. Here we present short‐term (7–65 days) responses of male red‐backed fairywrens Malurus melanocephalus to wildfire near the onset of the typical breeding season. Young males of this species are characterized by plastic expression of sexual plumage phenotypes depending on circulating testosterone and body condition. Using two populations with fairywren captures before and after separate wildfires we illustrate that wildfire suppressed molt into ornamented plumage. Neither baseline plasma corticosterone or furcular fat stores were affected by fire. However, fire seemed to interfere with the termporal increase in plasma testosterone during the pre‐breeding season, leading to a lower proportion of males molting into ornamented plumage. Collectively, these findings suggest that wildfires inhibit or greatly delay acquisition of ornamentation in males through enduring suppression of testosterone circulation.

Traffic noise alters individual social connectivity, but not space-use, of Red-backed Fairywrens

ABSTRACT The prevalence of human-generated noise is posing novel challenges to birds, by changing how they communicate or causing them to disperse away from the source of noise. We sought to understand how noise affected space-use and social connectivity in a small passerine bird, the Red-backed Fairywren (Malurus melanocephalus). As the displaced birds would likely be forced to occupy a smaller area that may already have resident individuals, we predicted that noise-affected birds would show increased social connectivity that may include new individuals. To test this, we introduced an experimental point-source of traffic noise to groups of fairywrens in an otherwise quiet habitat and compared the change in social connectivity of birds in groups exposed to noise to the changes in social connectivity in neighbouring groups unaffected by noise. Contrary to our prediction, noise-affected birds had reduced social connectivity during experimental noise treatments, as measured by weighted-degree, which was driven by a reduction of interactions with birds of neighbouring groups outside the noise zone. Additionally, we did not discern a change in space-use in response to our noise treatment. Therefore, we suggest that noise reduces the efficacy of signal transmission and detection in this species, resulting in the reduction of social connectivity between groups of this otherwise highly social songbird.

Testosterone regulates CYP2J19-linked carotenoid signal expression in male red-backed fairywrens (Malurus melanocephalus).

Carotenoid pigments produce most red, orange and yellow colours in vertebrates. This coloration can serve as an honest signal of quality that mediates social and mating interactions, but our understanding of the underlying mechanisms that control carotenoid signal production, including how different physiological pathways interact to shape and maintain these signals, remains incomplete. We investigated the role of testosterone in mediating gene expression associated with a red plumage sexual signal in red-backed fairywrens (Malurus melanocephalus). In this species, males within a single population can flexibly produce either red/black nuptial plumage or female-like brown plumage. Combining correlational analyses with a field-based testosterone implant experiment and quantitative polymerase chain reaction, we show that testosterone mediates expression of carotenoid-based plumage in part by regulating expression of CYP2J19, a ketolase gene associated with ketocarotenoid metabolism and pigmentation in birds. This is, to our knowledge, the first time that hormonal regulation of a specific genetic locus has been linked to carotenoid production in a natural context, revealing how endocrine mechanisms produce sexual signals that shape reproductive success.

First record of black feathering in a female Red-backed Fairy-wren Malurus melanocephalus under natural conditions

During the breeding season, male Red-backed Fairy-wrens Malurus melanocephalus can exhibit a spectrum of plumages from wholly black-and-red to entirely brown. By contrast, females generally appear completely brown, although observations of birds in the hand have revealed that some females also develop some red feathers. Here, we document, for the first time, observations of a female Red-backed Fairy-wren that has developed both black and red feathers under natural conditions. We explore possible explanations for this including whether changes to the individual’s hormonal milieu could be responsible for the unusual plumage that we observed.

Asymmetries in reproductive anatomy: insights from promiscuous songbirds

Abstract Directional asymmetry in gonad size is commonly observed in vertebrates and is particularly pronounced in birds, where the left testis is frequently larger than the right. The adaptive significance of directional asymmetry in testis size is poorly understood, and whether it extends beyond the testes (i.e. side-correspondent asymmetry along the reproductive tract) has rarely been considered. Using the Maluridae, a songbird family exhibiting variation in levels of sperm competition and directional testis asymmetry, yet similar in ecology and life history, we investigated the relative roles of side-correspondence and sperm competition on male reproductive tract asymmetry at both inter- and intraspecific levels. We found some evidence for side-correspondent asymmetry. Additionally, sperm competition influenced directional asymmetry at each end of the reproductive tract: species experiencing higher levels of sperm competition had a relatively larger right testis and relatively more sperm in the right seminal glomerus. Within red-backed fairy-wrens (Malurus melanocephalus), auxiliary males had relatively more sperm in the left seminal glomerus, in contrast to a right-bias asymmetry throughout the reproductive tract in breeding males. Given that the number of sperm is important for competitive fertilization success, our results suggest that sperm competition shapes reproductive asymmetries beyond testis size, with likely functional consequences for male reproductive success.

Red‐backed fairywrens adjust habitat use in response to dry season fires

AbstractFire disturbance in tropical savannas is integral to maintaining habitat heterogeneity and biodiversity, but its impact on avian species is highly variable. Savannas in northern Australia have recently been invaded by gamba grass (Andropogon gayanus), a perennial tussock grass that fuels late season fires at eight times the intensity of native vegetation. As gamba grass rapidly outcompetes native species and promotes more frequent and intense fires, it greatly decreases landscape heterogeneity and alters the effect of fire in tropical savannas. To investigate how a small passerine, the red‐backed fairywren (Malurus melanocephalus), responds to fire disturbance and gamba grass cover, we studied their fine‐scale habitat use throughout the dry season before and after a high intensity fire. We used two spatially distinct approaches, radio‐telemetry and a transect‐based population census, to quantify fairywren habitat use at the group and population level, respectively. Radio‐telemetry and transect surveys revealed no direct mortality associated with the severe bushfire during the middle of the study season, suggesting fairywrens are resilient in the short‐term to fire disturbance. Our results indicate that fairywrens are largely flexible in their habitat use – instead of relocating after fire, they re‐centre their home range around the most photosynthetically productive habitats, dominated by saplings. While we found substantial variation in habitat use among social groups, red‐backed fairywren groups generally avoided dense habitat areas dominated by mature gamba grass. We conclude that red‐backed fairywrens are resilient to fire and flexible in their habitat use in the short‐term; however, in the long‐term, gamba grass may pose a threat to population viability. The importance of flexible behavioural strategies in tropical passerines will increase as fire regimes are exacerbated by invasive species and climate change.

Acoustic and physical mate guarding have different effects on intruder behaviour in a duetting songbird

When males compete for mates, they often defend paternity through mate guarding. In addition to physical guarding, in vocal species, especially duetting birds, individuals may duet with their mates in order to guard them. The acoustic mate-guarding hypothesis posits that duetting deters rivals. We experimentally tested the effectiveness of physical and acoustic mate guarding in a duetting songbird, the red-backed fairy-wren, Malurus melanocephalus, using a novel variation of a classic removal experiment. We temporarily removed males, such that females received either no guarding (mate removed), or only acoustic guarding (mate removed, his duet response played from speaker). We found that rival intrusion rates were highest when all guarding was prevented, slightly lower when only acoustic guarding occurred and lowest when pairs were unmanipulated, and both physical and acoustic guarding occurred. This suggests that both guarding techniques deter intruders, but acoustic guarding less so. Intruder display rate during removals was higher than in unmanipulated trials, regardless of acoustic guarding. Results suggest that acoustic guarding may function as a long-range signal that reduces the likelihood of rival intrusion, but physical guarding is necessary to prevent rivals from courting mates. We confirm that physical and acoustic mate guarding serve as important components of intruder deterrence, although they act at different levels. Our study broadens our understanding of multimodal paternity assurance strategies.

Environmental disturbance increases social connectivity in a passerine bird.

Individual level response to natural and anthropogenic disturbance represents an increasingly important, but as yet little understood, component of animal behavior. Disturbance events often alter habitat, which in turn can modify behaviors of individuals in affected areas, including changes in habitat use and associated changes in social structure. To better understand these relationships, we investigated aspects of habitat selection and social connectivity of a small passerine bird, the red-backed fairywren (Malurus melanocephalus), before vs. after naturally occurring fire disturbance in Northern Territory, Australia. We utilized a social network framework to evaluate changes in social dynamics pre- vs. post-fire. Our study covered the non-breeding season in two consecutive years in which fires occurred, and individuals whose habitat was affected and those that were not affected by fire. Individuals in habitat affected by fires had stronger social ties (i.e. higher weighted degree) after fires, while those that were in areas that were not affected by fire actually had lower weighted degree. We suggest that this change in social connections may be linked to habitat. Before fires, fairywrens used habitat that had similar grass cover to available habitat plots randomly generated within our study site. Fire caused a reduction in grass cover, and fairywrens responded by selecting habitat with higher grass cover relative to random plots. This study demonstrates how changes in habitat and/or resource availability caused by disturbance can lead to substantive changes in the social environment that individuals experience.

Early-moulting Red-backed Fairywren males acquire ornamented plumage in the absence of elevated androgens

ABSTRACTSexual ornaments, including plumage ornamentation, are often studied during breeding periods even though signal development can take place months earlier. This temporal disconnect potentially obscures the proximate mechanisms that underlie signal expression and development. We studied the correlation between androgen levels and expression of ornamented plumage in adult Red-backed Fairywrens (Malurus melanocephalus) 4–6 months before breeding, when signal production occurs in some, usually older, males. We found that, during this period, ornamented males, unornamented males and females all had low plasma androgen levels that did not differ from each other. Variation in androgen levels was unrelated to phenotype or moult. These findings differ from previous research conducted immediately prior to breeding in a different population of this species, which used correlative and experimental work to demonstrate that testosterone induces prenuptial moult and acquisition of ornamented plumage in younger males. Our study demonstrates that mechanisms contributing to signal production may vary within and among populations in relation to temporal, age-dependent, or geographic parameters. These results highlight the complexity of hormonal pathways to signal production, and the importance of studying signal acquisition throughout the entire period when signals are produced, as studies conducted at different time points may have quantitatively different results.

Working with what you've got: unattractive males show greater mate-guarding effort in a duetting songbird.

When mates are limited, individuals should allocate resources to mating tactics that maximize fitness. In species with extra-pair paternity (EPP), males can invest in mate guarding, or, alternatively, in seeking EPP. Males should optimize fitness by adjusting investment according to their attractiveness to females, such that attractive males seek EPP, and unattractive males guard mates. This theory has received little empirical testing, leaving our understanding of the evolution of mating tactics incomplete; it is unclear how a male's relative attractiveness influences his tactics. We conducted observations and experiments on red-backed fairy-wrens (Malurus melanocephalus) to address this question. We found that older, more attractive (red-black) males sought EPP, whereas unattractive (brown) males invested in alternative tactics-physical and acoustic mate guarding. Younger red-black males used intermediate tactics. This suggests that males adopt mating tactics appropriate to their attributes. Males obtained similar reproductive success, suggesting these alternative tactics may maximize each male's paternity gain. Though it is likely that female choice also determines paternity, rather than just male tactics, we establish that the many interconnected components of a male's sexual phenotype influence the evolution of his decision-making rules, deepening our understanding of how mating tactics evolve under sexual selection.

Testosterone regulates scarlet plumage in red-backed fairy-wrens

As the days begin to lengthen and winter recedes for yet another year, many birds dust off their most glamorous plumage to attract a mate. Males often opt for ostentatious displays while females tend to the dowdier end of the spectrum. But what factors regulate the dramatic differences in avian regalia between males and females? Willow Lindsay from the University of Gothenburg, Sweden, explains that the hormones that regulate sexual differences were thought to play a key role in defining plumage patterns, but the precise role of individual hormones was less clear. As testosterone starts flowing in spring, male red-backed fairy-wrens (Malurus melanocephalus) shed their dreary brown feathers in favour of a vivid scarlet and glossy black coat, while the females retain their dingy brown and white plumage. So, Lindsay and Douglas Barron headed south to Queensland, Australia, to find out how the plumage of red-backed fairy-wrens altered after they received a testosterone implant.Initially, the males and females both looked drab; however, soon after the birds received the implant, the females moulted and began sprouting shorter male-like feathers. The females also produced a vibrant patch of red feathers on their backs, similar to the bright red streak on the males’ backs. In addition, the feathers on the crown, belly and breast of the females turned a shade of pinky-orange, which Lindsay said was: ‘Never previously documented on a red-backed fairy-wren’. Only one female went on to produce black feathers like those of the males, although the beaks of all of the females became darker. And when Lindsay and Barron injected some females with gonadotropin-releasing hormone, in a bid to naturally raise the birds’ testosterone levels, the females were unable to increase the levels of the hormone in their blood.So, it seems that testosterone is the hormone that regulates the production of the carotenoid pigments that produce the males’ scarlet plumage; however, the hormone was unable to elicit production of the jet-black melanin pigment that produces their distinctive dark feathers. It seems that the female fairy-wrens still maintain the essential hormone mechanism that allows the males to put on their gaudy display, although the females are unable to produce sufficient testosterone to trigger the masculine transformation.

Testosterone activates sexual dimorphism including male-typical carotenoid but not melanin plumage pigmentation in a female bird.

In males it is frequently testosterone (T) that activates the expression of sexually selected morphological and behavioral displays, but the role of T in regulating similar traits in females is less clear. Here, we combine correlational data with results from T and gonadotropin-releasing hormone (GnRH) manipulations in both sexes to assess the role of T in mediating sexually dimorphic coloration and morphology in the red-backed fairy-wren (Malurus melanocephalus). We show that: (1) natural variation in female expression of ornamental traits (darkened bills and red back feathers) is positively associated with age and circulating androgen titres, (2) females have the capacity to express most male-typical traits in response to exogenous T, including carotenoid-pigmented body plumage, shorter feathers, darkened bill and enlarged cloacal protuberance, but (3) appear constrained in production of male-typical melanin-pigmented plumage, and (4) low androgen levels during the pre-nuptial molt, probably because of low ovarian capacity for steroid production (or luteinizing hormone sensitivity), prevent females from developing male-like ornamentation. Thus, females appear to retain molecular mechanisms for hormonally regulated male-typical ornamentation, although these are rarely activated because of insufficient production of the hormonal signal.

Male Red-backed Fairywrens appear to enhance a plumage-based signal via adventitious molt

ABSTRACT Phenotypically plastic signals that can be altered in response to changing environmental conditions provide animals with the ability to dynamically signal their current condition or status. Such flexibility might also provide a means of avoiding potential trade-offs between signal components. Among birds, for example, both the timing of expression and the coloration of nuptial plumage are often thought to be honest signals of condition. However, because plumage is a relatively static signal type, birds that express condition-dependent plumage signals may face a trade-off between timing of signal production and signal quality, in that signals produced relatively early may be of lower quality because of seasonal constraints. A related cost may be increased fading or wear of plumage associated with extended duration of signal expression. Male Red-backed Fairywrens (Malurus melanocephalus) exhibit asynchronous development of nuptial red–black plumage, with some individuals molting into nuptial plumag...

Kin Signatures Learned in the Egg? Red-Backed Fairy-Wren Songs Are Similar to Their Mother's In-Nest Calls and Songs

Many vocal animals recognize kin using vocal cues, in territorial contexts and in rearing young, but little is known about the developmental and evolutionary mechanisms that produce vocal kin recognition systems. In the cooperatively breeding red-backed fairy-wren (Malurus melanocephalus), females give specific “in-nest calls” while incubating their eggs. Elements from these calls are incorporated into chicks’ begging calls, and appear to be used by parents for recognition. This is likely a result of an embryo’s ability to learn the call elements in the egg. Here, we explore the idea that maternal vocal elements may be incorporated into offspring’s adult songs, and serve as signatures of kinship, which would aid in kin recognition and benefit signaler and receiver. To investigate this hypothesis, we tested for similarities between maternal vocal elements (in-nest calls and songs) and songs of their adult offspring. We then determined whether offspring songs were more similar to the maternal vocalizations they heard only as embryos (in-nest calls), or maternal songs they heard throughout development, but mostly post-fledge (mothers’ full songs). We used dynamic time warping to compare maternal vocal elements with elements in their offspring’s adult songs. The elements of each offspring were more similar to the elements of their own mother than to the elements of any other female (but only for the average similarity score), suggesting they may serve as kin signatures. We also found that offspring song elements were more similar to their mother’s song elements than to their mother’s in-nest call elements. In addition, female in-nest call elements were more similar to their own song elements than to the song elements of any other female. Offspring that produced song elements highly similar to their mother’s song elements also had song elements highly similar to their mother’s in-nest call elements. Signals of kinship may function critically for survival and successful reproduction, by allowing an individual to allocate care and defense to kin and to avoid mating with genetic relatives. Understanding the processes that facilitate effective kin recognition, including development of kin signatures, helps us to understand how these crucial signaling systems may have evolved.