Candidate gene polymorphisms are linked to dispersive and migratory behaviour: Searching for a mechanism behind the "paradox of the great speciators".

The "paradox of the great speciators" has puzzled evolutionary biologists for over half a century. A great speciator requires excellent dispersal propensity to explain its occurrence on multiple islands, but reduced dispersal ability to explain its high number of subspecies. A rapid reduction in dispersal ability is often invoked to solve this apparent paradox, but a proximate mechanism has not been identified yet. Here, we explored the role of six genes linked to migration and animal personality differences (CREB1, CLOCK, ADCYAP1, NPAS2, DRD4, and SERT) in 20 South Pacific populations of silvereye (Zosterops lateralis) that range from highly sedentary to partially migratory, to determine if genetic variation is associated with dispersal propensity and migration. We detected genetic associations in three of the six genes: (i) in a partial migrant population, migrant individuals had longer microsatellite alleles at the CLOCK gene compared to resident individuals from the same population; (ii) CREB1 displayed longer average microsatellite allele lengths in recently colonized island populations (<200 years), compared to evolutionarily older populations. Bayesian broken stick regression models supported a reduction in CREB1 length with time since colonization; and (iii) like CREB1, DRD4 showed differences in polymorphisms between recent and old colonizations but a larger sample is needed to confirm. ADCYAP1, SERT, and NPAS2 were variable but that variation was not associated with dispersal propensity. The association of genetic variants at three genes with migration and dispersal ability in silvereyes provides the impetus for further exploration of genetic mechanisms underlying dispersal shifts, and the prospect of resolving a long-running evolutionary paradox through a genetic lens.

A new candling procedure for thick and opaque eggs and its application to avian conservation management.

The ability to monitor developing avian embryos and their associated vascular system via candling enables the application of important reproductive management techniques. Egg candling facilitates the confirmation of egg viability throughout the incubation process and identification of a precise position on a vein for the safe extraction of blood. Blood samples may then be analysed to retrieve vital health and genetic information to assist in conservation management. However, the thick or opaque egg shell characteristics of some avian species prevents the observation of egg contents using traditional candling methods, thus limiting management options. This paper tests a novel method of preparing thick-shelled or opaque eggs so that traditional egg candling and blood extraction methods may be applied. Eggs from captive emu (Dromaius novaehollandiae, Latham 1790) and southern cassowary (Casuarius casuarius johnsonii, Linnaeus 1758) were obtained, and partial fenestration was performed on two areas of shell either before incubation or at ⅓ of incubation. Hatchability and weight loss were examined as a measure of effect of the fenestration process on the developing embryo. Clear observation of vascular development was successful in 97% of viable fenestrated eggs, without affecting hatchability or weight loss. Blood samples were taken from developing embryos and DNA was successfully extracted for proof of concept of this new technique. The ability to observe vascular development and monitor the developing embryo in thick and opaque eggs will significantly improve both in situ and ex situ population management options such as in ovo sexing in species of concern.

Use of anthropogenic-related nest material and nest parasite prevalence have increased over the past two centuries in Australian birds.

Global plastic production has increased exponentially since the 1940s, resulting in the increased presence of anthropogenic debris in the environment. Recent studies have shown that birds incorporate anthropogenic debris into their nests, which can reduce nest ectoparasite loads. However, we know little about the long-term history of interactions among birds, anthropogenic debris, and ectoparasites. Our study took a unique approach to address this issue by determining the prevalence of anthropogenic debris and ectoparasitic nest flies (Protocalliphora and Passeromyia spp.) in 893 bird nests from 224 species between 1832 and 2018, which were sourced from Australian museum collections. The prevalence of anthropogenic material increased from approximately 4% in 1832 to almost 30% in 2018. This change was driven by an increase in the incorporation of synthetic rather than biodegradable anthropogenic debris (by 2018 ~ 25% of all nests contained synthetics), with the first synthetic item being found in a nest from 1956 in the city of Melbourne. Nest parasite prevalence increased over time but contrary to other studies, there was no relationship between habitat type or anthropogenic material and parasite presence. Our study is the first to use museum specimens to quantify temporal and spatial impacts of anthropogenic material on birds, the results of which justifies contemporary concerns regarding the ubiquitous nature of human impacts on terrestrial wildlife.

Coping with a changing soundscape: avoidance, adjustments and adaptations.

Since the industrial age, background anthropogenic noise has become a pervasive feature of many habitable environments. This relatively recent environmental feature can be particularly challenging for organisms that use acoustic forms of communication due to its propensity for masking and decreasing the potential acoustic space of signals. Furthermore, anthropogenic noise may affect biological processes including animal interactions, physiological and behavioural responses to stimuli and cognitive development. However, animals' cognitive abilities may enable them to cope with high levels of anthropogenic noise through learning, the employment of acoustic and behavioural flexibility as well as the use of multi-modal sensory systems. We are only just beginning to understand how neural structures, endocrine systems and behaviour are mechanistically linked in these scenarios, providing us with information we can use to mitigate deleterious effects of pervasive noise on wildlife, along with highlighting the remarkable adaptability of animals to an increasingly anthropogenic world. In this review, I will focus mainly on birds, due to the amount of literature on the topic, and survey recent advancements made in two main spheres: (1) how anthropogenic noise affects cognitive processes and (2) how cognition enables animals to cope with increasingly noisy environments. I will be highlighting current gaps in our knowledge, such as how noise might impact behavioural traits such as predation, as well as how noise causes physical damage to neurotransmitters and affects stress levels, in order to direct future studies on this topic.

Social inheritance of avoidances shapes the structure of animal social networks.

Social structure can have significant effects on selection, affecting both individual fitness traits and population-level processes. As such, research into its dynamics and evolution has spiked in the last decade, where theoretical and computational advances in social network analysis have increased our understanding of its ecological and inheritance underpinnings. Yet, the processes that shape the formation of structure within social networks are poorly understood and the role of social avoidances unknown. Social avoidances are an alternate of social affiliation in animal societies, which, although invisible, likely play a role in shaping animal social networks. Assuming social avoidances evolve under similar constraints as affiliative behavior, we extended a previous model of social inheritance of affiliations to investigate the impact of social inheritance of avoidances on social network structure. We modeled avoidances as relationships that individuals can copy from their mothers or from their mother's social environment and varied the degrees to which individuals inherit social affiliates and avoidances to test their combined influence on social network structure. We found that inheriting avoidances via maternal social environments made social networks less dense and more modular, thereby demonstrating how social avoidance can shape the evolution of animal social networks.

Mitochondrial Genome Fragmentation Occurred Multiple Times Independently in Bird Lice of the Families Menoponidae and Laemobothriidae.

Mitochondrial (mt) genome fragmentation has been discovered in all five parvorders of parasitic lice (Phthiraptera). To explore whether minichromosomal characters derived from mt genome fragmentation are informative for phylogenetic studies, we sequenced the mt genomes of 17 species of bird lice in Menoponidae and Laemobothriidae (Amblycera). Four species of Menoponidae (Actornithophilus sp. 1 ex [pied oystercatcher], Act. sp. 2 ex [masked lapwing], Austromenopon sp. 2 ex [sooty tern and crested tern], Myr. sp. 1 ex [satin bowerbird]) have fragmented mt genomes, whereas the other 13 species retain the single-chromosome mt genomes. The two Actornithophilus species have five and six mt minichromosomes, respectively. Aus. sp. 2 ex [sooty tern and crested tern] has two mt minichromosomes, in contrast to Aus. sp. 1 ex [sooty shearwater], which has a single mt chromosome. Myr. sp. 1 ex [satin bowerbird] has four mt minichromosomes. When mapped on the phylogeny of Menoponidae and Laemobothriidae, it is evident that mt genome fragmentation has occurred multiple times independently among Menoponidae and Laemobothriidae species. We found derived mt minichromosomal characters shared between Myrsidea species, between Actornithophilus species, and between and among different ischnoceran genera, respectively. We conclude that while mt genome fragmentation as a general feature does not unite all the parasitic lice that have this feature, each independent mt genome fragmentation event does produce minichromosomal characters that can be informative for phylogenetic studies of parasitic lice at different taxonomic levels.

Unexpected Pathogen Diversity Detected in Australian Avifauna Highlights Potential Biosecurity Challenges.

Birds may act as hosts for numerous pathogens, including members of the family Chlamydiaceae, beak and feather disease virus (BFDV), avipoxviruses, Columbid alphaherpesvirus 1 (CoAHV1) and Psittacid alphaherpesvirus 1 (PsAHV1), all of which are a significant biosecurity concern in Australia. While Chlamydiaceae and BFDV have previously been detected in Australian avian taxa, the prevalence and host range of avipoxviruses, CoAHV1 and PsAHV1 in Australian birds remain undetermined. To better understand the occurrence of these pathogens, we screened 486 wild birds (kingfisher, parrot, pigeon and raptor species) presented to two wildlife hospitals between May 2019 and December 2021. Utilising various qPCR assays, we detected PsAHV1 for the first time in wild Australian birds (37/486; 7.61%), in addition to BFDV (163/468; 33.54%), Chlamydiaceae (98/468; 20.16%), avipoxviruses (46/486; 9.47%) and CoAHV1 (43/486; 8.85%). Phylogenetic analysis revealed that BFDV sequences detected from birds in this study cluster within two predominant superclades, infecting both psittacine and non-psittacine species. However, BFDV disease manifestation was only observed in psittacine species. All Avipoxvirus sequences clustered together and were identical to other global reference strains. Similarly, PsAHV1 sequences from this study were detected from a series of novel hosts (apart from psittacine species) and identical to sequences detected from Brazilian psittacine species, raising significant biosecurity concerns, particularly for endangered parrot recovery programs. Overall, these results highlight the high pathogen diversity in wild Australian birds, the ecology of these pathogens in potential natural reservoirs, and the spillover potential of these pathogens into novel host species in which these agents cause disease.

Geographically pervasive effects of urban noise on frequency and syllable rate of songs and calls in silvereyes (Zosterops lateralis).

Recent studies in the Northern Hemisphere have shown that songbirds living in noisy urban environments sing at higher frequencies than their rural counterparts. However, several aspects of this phenomenon remain poorly understood. These include the geographical scale over which such patterns occur (most studies have compared local populations), and whether they involve phenotypic plasticity or microevolutionary change. We conducted a field study of silvereye (Zosterops lateralis) vocalizations over more than 1 million km(2) of urban and rural south-eastern Australia, and compared possible effects of urban noise on songs (which are learned) and contact calls (which are innate). Across 14 paired urban and rural populations, silvereyes consistently sang both songs and contact calls at higher frequencies in urban environments. Syllable rate (syllables per second) decreased in urban environments, consistent with the hypothesis that reflective structures degrade song and encourage longer intervals between syllables. This comprehensive study is, to our knowledge, the first to demonstrate varied adaptations of urban bird vocalizations over a vast geographical area, and to provide insight into the mechanism responsible for these changes.

Limited effects of traffic noise on behavioural responses to conspecific mating calls in the eastern sedge frog Litoria fallax.

Anthropogenic noise is a pervasive environmental feature across both urban and non-urban habitats and presents a novel challenge especially for acoustically communicating species. While it is known that some species adjust acoustic signals to communicate more effectively in noisy habitats, we know very little about how the receivers of these signals might be impacted by anthropogenic noise. Here, we investigated female and male Litoria fallax frogs' ability to distinguish between high- and low-quality acoustic signals during the presence of background traffic noise and without. We performed a controlled behavioural experiment whereby frogs were presented with simultaneously broadcasted attractive and unattractive calls from opposing directions, once with background traffic noise and once without. We found that females in particular chose the unattractive call significantly more often (and males significantly less often) when noise was being broadcast. This indicates that anthropogenic noise potentially affects receiver responses to acoustic signals, even when calls are not acoustically masked, with potential consequences for maladaptive mating behaviours and population outcomes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10211-021-00378-7.

Diversity begets diversity: A global perspective on gender equality in scientific society leadership.

Research shows that gender inequality is still a major issue in academic science, yet academic societies may serve as underappreciated and effective avenues for promoting female leadership. That is, society membership is often self-selective, and board positions are elected (with a high turnover compared to institutions)-these characteristics, among others, may thus create an environment conducive to gender equality. We therefore investigate this potential using an information-theoretic approach to quantify gender equality (male:female ratios) in zoology society boards around the world. We compare alternative models to analyze how society characteristics might predict or correlate with the proportion of female leaders, and find that a cultural model, including society age, size of board and whether or not a society had an outward commitment or statement of equality, was the most informative predictor for the gender ratio of society boards and leadership positions. This model was more informative than alternatives that considered, for instance, geographic location, discipline of study or taxonomic focus. While women were more highly represented in society leadership than in institutional academic leadership, this representation was still far short of equal (~30%): we thus also provide a checklist and recommendations for societies to contribute to global gender equality in science.

Birds Learn Socially to Recognize Heterospecific Alarm Calls by Acoustic Association.

Animals in natural communities gain information from members of other species facing similar ecological challenges [1-5], including many vertebrates that recognize the alarm calls of heterospecifics vulnerable to the same predators [6]. Learning is critical in explaining this widespread recognition [7-13], but there has been no test of the role of social learning in alarm-call recognition, despite the fact that it is predicted to be important in this context [14, 15]. We show experimentally that wild superb fairy-wrens, Malurus cyaneus, learn socially to recognize new alarm calls and can do so through the previously undemonstrated mechanism of acoustic-acoustic association of unfamiliar with known alarm calls. Birds were trained in the absence of any predator by broadcasting unfamiliar sounds, to which they did not originally flee, in combination with a chorus of conspecific and heterospecific aerial alarm calls (typically given to hawks in flight). The fairy-wrens responded to the new sounds after training, usually by fleeing to cover, and responded equally as strongly in repeated tests over a week. Control playbacks showed that the response was not due simply to greater wariness. Fairy-wrens therefore learnt to associate new calls with known alarm calls, without having to see the callers or a predator. This acoustic-acoustic association mechanism of social learning could result in the rapid spread of alarm-call recognition in natural communities, even when callers or predators are difficult to observe. Moreover, this mechanism offers potential for use in conservation by enhancing training of captive-bred individuals before release into the wild.

Identifying hybridization and admixture using SNPs: application of the DArTseq platform in phylogeographic research on vertebrates.

Next-generation sequencing (NGS) approaches are increasingly being used to generate multi-locus data for phylogeographic and evolutionary genetics research. We detail the applicability of a restriction enzyme-mediated genome complexity reduction approach with subsequent NGS (DArTseq) in vertebrate study systems at different evolutionary and geographical scales. We present two case studies using SNP data from the DArTseq molecular marker platform. First, we used DArTseq in a large phylogeographic study of the agamid lizard Ctenophorus caudicinctus, including 91 individuals and spanning the geographical range of this species across arid Australia. A low-density DArTseq assay resulted in 28 960 SNPs, with low density referring to a comparably reduced set of identified and sequenced markers as a cost-effective approach. Second, we applied this approach to an evolutionary genetics study of a classic frog hybrid zone (Litoria ewingii-Litoria paraewingi) across 93 individuals, which resulted in 48 117 and 67 060 SNPs for a low- and high-density assay, respectively. We provide a docker-based workflow to facilitate data preparation and analysis, then analyse SNP data using multiple methods including Bayesian model-based clustering and conditional likelihood approaches. Based on comparison of results from the DArTseq platform and traditional molecular approaches, we conclude that DArTseq can be used successfully in vertebrates and will be of particular interest to researchers working at the interface between population genetics and phylogenetics, exploring species boundaries, gene exchange and hybridization.

Experimental exposure to urban and pink noise affects brain development and song learning in zebra finches (Taenopygia guttata).

Recently, numerous studies have observed changes in bird vocalizations-especially song-in urban habitats. These changes are often interpreted as adaptive, since they increase the active space of the signal in its environment. However, the proximate mechanisms driving cross-generational changes in song are still unknown. We performed a captive experiment to identify whether noise experienced during development affects song learning and the development of song-control brain regions. Zebra finches (Taeniopygia guttata) were bred while exposed, or not exposed, to recorded traffic urban noise (Study 1) or pink noise (Study 2). We recorded the songs of male offspring and compared these to fathers' songs. We also measured baseline corticosterone and measured the size of song-control brain regions when the males reached adulthood (Study 1 only). While male zebra finches tended to copy syllables accurately from tutors regardless of noise environment, syntax (the ordering of syllables within songs) was incorrectly copied affected by juveniles exposed to noise. Noise did not affect baseline corticosterone, but did affect the size of brain regions associated with song learning: these regions were smaller in males that had been had been exposed to recorded traffic urban noise in early development. These findings provide a possible mechanism by which noise affects behaviour, leading to potential population differences between wild animals occupying noisier urban environments compared with those in quieter habitats.

The relative roles of cultural drift and acoustic adaptation in shaping syllable repertoires of island bird populations change with time since colonization.

In birds, song divergence often precedes and facilitates divergence of other traits. We assessed the relative roles of cultural drift, innovation, and acoustic adaptation in divergence of island bird dialects, using silvereyes (Zosterops lateralis). In recently colonized populations, syllable diversity was not significantly lower than source populations, shared syllables between populations decreased with increasing number of founder events, and dialect variation displayed contributions from both habitat features and drift. The breadth of multivariate space occupied by recently colonized Z. l. lateralis populations was comparable to evolutionarily old forms that have diverged over thousands to hundreds of thousands of years. In evolutionarily old subspecies, syllable diversity was comparable to the mainland and the amount of variation in syllable composition explained by habitat features increased by two- to threefold compared to recently colonized populations. Together these results suggest that cultural drift influences syllable repertoires in recently colonized populations, but innovation likely counters syllable loss from colonization. In evolutionarily older populations, the influence of acoustic adaptation increases, possibly favoring a high diversity of syllables. These results suggest that the relative importance of cultural drift and acoustic adaptation changes with time since colonization in island bird populations, highlighting the value of considering multiple mechanisms and timescale of divergence when investigating island song divergence.

Traffic noise affects embryo mortality and nestling growth rates in captive zebra finches.

Over the past two decades, studies of songbird populations have detected decreases in the reproductive success of individuals living in urban areas. Anthropogenic noise is considered to be particularly detrimental, however the exact relationship between noise and reproductive success is still unclear because noise is often correlated with many other detrimental factors (e.g., predation, reduced territory quality). We used an experiment to specifically test the effects of urban noise on reproduction of captive zebra finches (Taeniopygia guttata). We found that latency to breed and the size of successfully fledged clutches were consistent between groups, however success of initial nesting attempts was reduced by traffic noise. Further, this reduced success leading to increased numbers of nesting attempts by birds in the noise condition was due to higher levels of embryo mortality in the traffic noise treatment group, which also suffered a lag in nestling growth rates during the first two weeks post-hatch. While parental baseline circulating corticosterone was not chronically affected by noise treatment, we identified some interaction effects whereby certain reproductive measures (laying latency and clutch size) were most strongly affected by treatment when mothers had higher levels of baseline corticosterone. These results indicate that traffic noise may reduce reproductive success through changes in parental behaviour, and that traffic noise may disproportionately affect chronically stressed individuals during reproduction. J. Exp. Zool. 323A: 722-730, 2015. © 2015 Wiley Periodicals, Inc.

Song convergence in multiple urban populations of silvereyes (Zosterops lateralis).

Recent studies have revealed differences between urban and rural vocalizations of numerous bird species. These differences include frequency shifts, amplitude shifts, altered song speed, and selective meme use. If particular memes sung by urban populations are adapted to the urban soundscape, "urban-typical" calls, memes, or repertoires should be consistently used in multiple urban populations of the same species, regardless of geographic location. We tested whether songs or contact calls of silvereyes (Zosterops lateralis) might be subject to such convergent cultural evolution by comparing syllable repertoires of geographically dispersed urban and rural population pairs throughout southeastern Australia. Despite frequency and tempo differences between urban and rural calls, call repertoires were similar between habitat types. However, certain song syllables were used more frequently by birds from urban than rural populations. Partial redundancy analysis revealed that both geographic location and habitat characteristics were important predictors of syllable repertoire composition. These findings suggest convergent cultural evolution: urban populations modify both song and call syllables from their local repertoire in response to noise.