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Griffith, S. C.

Publications and source records attributed to Griffith, S. C..

12 recordsLinked to original sources

Sensitive period for song learning outlasts parent-offspring cohesion in wild zebra finches

Communication is central to social behaviour, with vocalisations playing a crucial role in many species. In some species, vocalisations are learned, with songbirds being key to understanding vocal learning. The Australian zebra finch (Taeniopygia castanotis) is the most studied model organism for vocal learning. In captivity, juveniles are typically housed with their father, where males learn their father song and females develop a preference for that song. In nature, however, the social structure of zebra finches is more dynamic across space and time. To identify the natural social conditions during song learning, we followed zebra finch families across their early life in the wild using automated radio-tracking. The distance between juveniles and their parents increased post-fledging and became similar to the distance between juveniles and unrelated adults by the second half of the song learning period. These findings indicate a highly dynamic social environment during the song learning period and suggest that juvenile males could learn from many tutors and that females may develop broader song preferences. Thus, studies based on one-tutor paradigms should be interpreted carefully with respect to functional implications and highlight that future vocal learning studies could better reflect the social conditions under which song develops.

animal behavior and cognition↗

Communication networks of wild zebra finches (Taeniopygia castanotis)

Communication networks are widespread across species, permitting information flow and facilitating social connections across space and time. In birds, communication networks are well studied in territorial species with long-range songs connecting individuals across space, where unintended listeners extract information from others signalling interactions. Yet, acoustic signals also play important social roles at short range, forming communication networks that connect individuals within larger social units. Wild zebra finches (Taeniopygia castanotis) provide a unique model system to examine such communication networks in a non-territorial species. Zebra finches breed in loose colonies in the Australian arid zone, move around in pairs or small groups, and gather at social hotspots, thus forming dynamic, potentially multi-level, societies. Here, we quantified singing activity and connectivity using the individually distinctive male song recorded at two breeding sub-colonies and three social hotspots over one to three days. We identified 1,835 song bouts from 163 males based on spectrographic similarities and we assessed within and between individual song assignments with a deep learning model (BirdNET). We constructed communication networks based on temporal singing proximity at shared locations: social hotspots and breeding colonies. We reveal higher singing activity at social hotspots than at breeding sites, with almost no dawn song at either site. Singing peaked later, yet at different times of day between breeding sites and social hotspots. Communication networks, with distinct males singing in close temporal proximity, were apparent in both contexts, with larger networks at hotspots. These networks included some individuals that sang together repeatedly at either site, but overall networks were not strongly nested, with only very few males maintaining associations across breeding colonies and hotspots. These networks may facilitate synchronised foraging and breeding as adaptations to a harsh and unpredictable environment. Additionally, our approach offers a novel road map for widening the understanding of communication networks.

animal behavior and cognition↗

Programmed DNA elimination drives rapid genomic innovation in two thirds of all bird species

Bird genomes are among the most stable in terms of synteny and gene content across vertebrates. However, germline-restricted chromosomes (GRCs) represent a striking exception where programmed DNA elimination confines large-scale genomic changes to the germline. GRCs are known to occur in songbirds (oscines), but have been studied only in a few species of Passerides such as the zebra finch, the key model for passerine genomics. Their presence and evolutionary dynamics in most major passerine lineages remain largely unexplored, with suboscines entirely unexamined by cytogenetic or genomic methods. Here, we present the most comprehensive comparative analysis of GRCs to date, spanning 44 million years of passerine evolution. By generating the first germline reference genomes of an oscine and a suboscine, 22 novel germline draft genomes spanning nearly all major passerine lineages and a germline draft genome of a parrot outgroup, we show that the GRC is likely present in 6,700 passerine species. Our results reveal that the GRC evolves rapidly and distinctly from the standard A chromosomes (autosomes and sex chromosomes), yet retains functionally important, selectively maintained genes. We observed gene and repeat turnover occuring orders of magnitude faster than on the A chromosomes. Some GRC genes, such as cpeb1 and pim1, are widespread from an ancient duplication. In contrast, other GRC genes, like mfsd2b and bmp15, have been independently duplicated onto the GRC multiple times, suggesting adaptive constraints. The discovery of zglp1 on the zebra finch GRC, initially copied from chromosome 30 and subsequently lost from it, indicates functional replacement, where the GRC permits gene loss from the standard genome. As the GRC harbors the only zglp1 copy in most of the [~]4000 Passerides species, GRC loss would compromise essential germline functions. Our findings establish the GRC as a genomic innovator driving rapid germline evolution. This fact highlights its evolutionary significance for passerine diversification and suggests that programmed DNA elimination may be an overlooked yet phylogenetically widespread mechanism in many understudied animal lineages.

genomics↗

Recent divergence and microgeographic genetic structure in an endangered Australian songbird: the southern black-throated finch

Anthropogenic habitat loss and climate change threaten global biodiversity. Effective conservation management requires a detailed understanding of geographic structure, genetic diversity, and demography of threatened species. The black-throated finch, Poephila cincta, is an Australian songbird with two subspecies: atropygialis and cincta. The southern subspecies, cincta, has experienced an [~]80% range contraction over the last century and is listed as endangered but genetic surveys of it are incomplete. Here, we use a combination of reduced representation and whole genome sequencing to examine genetic differentiation, spatial genetic structure, and demographic history in both forms of this species. We find that atropygialis and cincta are genetically distinct despite a history of divergence with gene flow and geographically isolated by a biogeographic barrier known as the Einasleigh Uplands. Since they last shared a common ancestor [~]400,000 years ago, the two subspecies have experienced distinct demographic trajectories: population expansion in atropygialis and population decline in cincta. We find that the two remnant population centers of cincta, from the Galilee Basin and the Townsville Coastal Plain, each represent genetically distinct lineages that last shared appreciable levels of gene flow [~]4,000 years ago. Moreover, we report striking microgeographic genetic structure from the Townsville Coastal Plain between populations <20 km apart associated with barriers to dispersal caused by anthropogenic habitat modification over the last 50 years: namely the construction of the Ross River Dam. Our findings highlight the urgent need for a conservation approach that prioritizes habitat restoration to re-establish population connectivity in the endangered southern black-throated finch.

evolutionary biology↗

Zebra finches produce intralaryngeal laminar flow whistles during panting

Birds and mammals converged upon the same physical mechanism of vocal fold vibration to produce their broad range of voiced sounds critical to communication1. The frequency range of vocal fold vibration is limited per species by biophysical constraints to 3-4 octaves2. However, recent work reported vocalizations in zebra finches with apparent fundamental frequencies of 7-11 kHz3 that far exceed the range of regular calls and song (0.5-1.5 kHz)4,5. These "heat" or "incubation" calls are suggested to have close-range communicative relevance in the global temperature rise context3,6, but their acoustics are poorly described and by what biophysical mechanism they are produced remains unknown. We recorded heat calls in adult zebra finches in vivo and show they are extremely soft, frequency-modulated calls with source levels of 13.9 {+/-} 3.3 dB SPL at one meter with dominant frequencies of 6.8 {+/-} 0.6 kHz. Through a series of in vitro experiments, we establish that these calls are aerodynamic whistles produced inside the avian larynx, not syrinx, during inspiration. Respiratory air flow during whistle production is an order of magnitude higher than song and consistent with thermal panting for evaporative cooling6,7. Laryngeal geometry and dimensional flow analysis suggest that these whistles are laminar flow whistles that occur when a flow boundary layer is in a transition phase from laminar to turbulent flows8,9. Birds, like some rodents10-12, are thus able to produce both voiced sounds and aerodynamical whistles in their vocal tract.

physiology↗

Independent evolution of atypical sperm morphology in a passerine bird, the red-browed finch (Neochmia temporalis temporalis)

Spermatozoa exhibit striking morphological variation across the animal kingdom. In passerine birds, sperm exhibit considerable variation in size, yet the basic sperm phenotype is highly conserved; sperm are filiform, the head is corkscrew-shaped, and the midpiece is elongated and twisted around the flagellum. A significant departure from this typical sperm morphology has been reported in the sister species, the Eurasian bullfinch (Pyrrhula pyrrhula) and Azores bullfinch (P. murina). Here, we report a second evolutionary shift in passerine sperm phenotype in the nominate subspecies of the red-browed finch (Neochmia temporalis temporalis); sperm are non-filiform, with an ellipsoid head, and an extremely short midpiece restricted to the nuclear-axoneme junction. Additionally, we show that the sperm phenotype of the red-browed finch is similar to the putatively neotenous sperm described in the two bullfinch species. Using whole-genome data, we found no evidence that the unusual sperm phenotype of the red-browed finch is associated with reduced genetic variation or a population bottleneck. In contrast, we find some support for the hypothesis that relaxed post-copulatory sexual selection may, at least in part, explain the unusual sperm of the red-browed finch. We also discuss the possible roles of mutation, genetic drift, and genetic hitchhiking, in the evolutionary origins and maintenance of neotenous sperm phenotypes. Finally, we suggest that these dramatic evolutionary shifts in sperm phenotype warrant further investigation and highlight the need for a greater understanding of the developmental and genomic basis of sperm phenotype.

evolutionary biology↗

Diversifying selection and adaptive introgression of carotenoid-processing genes underlie the evolution of bill color in the long-tailed finch

Carotenoid pigmentation produces the yellow and red coloration of birds and other vertebrates, but our understanding of the genetic architecture of carotenoid ornamentation is largely limited to studies of novel color variants observed in captively bred populations. The complexity of carotenoid-based color evolution in nature remains poorly characterized. Here, we examine the long-tailed finch Poephila acuticauda, an Australian songbird with two hybridizing subspecies that differ in bill coloration: yellow in western subspecies acuticauda and red in eastern subspecies hecki. We characterize the carotenoid composition of each subspecies and find that yellow bills can be explained by the loss of C(4)-oxidation, thus blocking yellow dietary pigments from being metabolized to red. Combining linked-read genomic sequencing and reflectance spectrophotometry measurements of bill color collected from wild-sampled finches and laboratory crosses, we identify four loci that together explain 53% of variance in this trait. The two loci of largest effect contain the genes CYP2J19, an essential enzyme for the ketolation via C(4)-oxidation of dietary carotenoids, and TTC39B, an enhancer of ketocarotenoid production. Evolutionary genealogy reconstruction indicates that the red-billed phenotype is ancestral and yellow alleles at both CYP2J19 and TTC39B arose and fixed in acuticauda approximately 100 kya. Yellow alleles then introgressed into hecki less than 5 kya. Across all four loci, acuticauda derived variants show evidence of selective sweeps, implying that yellow bill coloration has been favored by natural selection. Our study suggests that the frequent adaptive evolutionary transitions between red and yellow ornamentation in nature can have a simple genetic basis. SignificanceWe studied variation in carotenoid ornamentation of an Australian songbird with two hybridizing subspecies that differ in bill color: one yellow and the other red. We identified a single metabolic process, C(4)-oxidation, underlying the distinct carotenoid composition of these two bill colors. Genetic association mapping revealed four major effect loci that explained most of the observed variation the trait, including the oxidative ketolation enzyme CYP2J19 and the carotenoid ketolation enhancer gene TTC39B. Evolutionary reconstruction indicates that yellow alleles are derived, ancient (~100 kya), and under positive selection. This has driven their recent (<5 kya) adaptive introgression across the hybrid zone. These findings have important implications for understanding the role of natural selection in phenotypic evolution in natural systems.

evolutionary biology↗

Mitonuclear interactions impact aerobic metabolism in hybrids and may explain mitonuclear discordance in young, naturally hybridizing bird lineages

Understanding genetic incompatibilities and genetic introgression between incipient species are major goals in evolutionary biology. Mitochondrial genes evolve rapidly and exist in dense gene networks with coevolved nuclear genes, suggesting that mitochondrial respiration may be particularly susceptible to disruption in hybrid organisms. Mitonuclear interactions have been demonstrated to contribute to hybrid disfunction between deeply divergent taxa crossed in the laboratory, but there are few empirical examples of mitonuclear interactions between younger lineages that naturally hybridise. Here we use experimental crosses and high resolution respirometry to provide the first evidence in a bird that inter-lineage mitonuclear interactions impact mitochondrial aerobic metabolism. Specifically, respiration capacity of the two paternal backcrosses (with mismatched mito-nuclear combinations) differ from one another, although they do not differ to the parental groups or maternal backcrosses as we would expect of mitonuclear disruptions. In the wild hybrid zone between these subspecies the mitochondrial cline centre is shifted west of the nuclear cline centre, which is consistent with the direction of our experimental results. Our results therefore demonstrate asymmetric mitonuclear interactions that impact the capacity of cellular mitochondrial respiration and may help to explain the geographic discordance between mitochondrial and nuclear genomes observed in the wild.

evolutionary biology↗

Environmental Uncertainty Affects Movement and Space-use in Sheep

Animals constantly experience periods of uncertainty due to seasonal changes in food distribution. The changing climate results in more variable weather patterns, which in turn alter environmental conditions, and can result in resource distribution being less predictable in space and time. How animals respond to these uncertain conditions, in particular the changing distribution of food resources, remains largely unclear and is an important question in the field of movement and animal ecology. Here we used an experimental approach to study how Merino sheep (Ovis aries) responded to different levels of environmental uncertainty in a drought-impacted region of the Australian arid zone. Sheep were unfamiliar with the experimental resource distribution at the start and progressively decreased their uncertainty (i.e., increased their environmental knowledge) when discovering an increasing number of foraging patches. We tracked 50 sheep with GPS collars (1 location every 15 sec) and deduced their movement and space use behaviour. When environmental uncertainty decreased, individuals moved more directionally (greater step length, smaller turn angles) and moved greater distances per day. They also had larger daily home ranges but rested in similar areas on consecutive nights (similar displacement, with the exception when five patches were discovered). Our study demonstrates how an arid zone, free-ranging ungulate adjusts its movement and space use behaviour as it gains environmental information in order to forage efficiently during periods of uncertainty. Our study provides important insights into how animals cope with variable environments and different levels of uncertainty.

animal behavior and cognition↗

Heat stress conditions affect the social network structure of free-ranging sheep

Extreme weather conditions, like heatwave events, are becoming more frequent with climate change. Animals often modify their behaviour to cope with environmental changes and extremes. If the environmental conditions influence the trade-off between an individuals social propensity and optimal thermoregulation through shade use for instance, then divergent social decisions may be made. Hence, such behavioural changes have the potential to influence an individuals position in its social network, and the social network structure as a whole. We investigated whether heat stress conditions (quantified through the Temperature Humidity Index) and the resulting use of shaded areas, influences the social network structure and an individuals position in it. We studied this in free-ranging sheep in the arid zone of Australia, GPS-tracking all 48 individuals in a flock. When heat stress conditions worsened, individuals spent more time in the shade and the network was more connected (higher density) and less modular. Furthermore, an individuals social connectivity scaled with its shade use behaviour. Interestingly, individuals with intermediate shade use were most strongly connected (degree, strength, betweeness), indicating their importance for the connectivity of the social network during heat stress conditions. Our study shows that heat stress conditions, which are predicted to increase in severity and frequency due to climate change, influence the resource use within the ecological environment. This has flow on effects for the animals social environment through the changed social network structure. Significance statementDue to climate change, animals experience heat stress conditions more frequently. When ambient temperatures are high, individuals can seek shaded areas to mitigate the effect. However, whether these behavioural changes affect the interaction patterns in social species is not well understood. We tracked all individuals in a flock of sheep using GPS collars. We demonstrate that when heat stress conditions worsened (higher temperature humidity index), individuals spent more time in the shade and the social network was more connected with less internal structure. Furthermore, an individuals social connectivity scaled with its shade use behaviour, and individuals with intermediate shade use were most strongly connected in their social network. Our findings illustrate that individuals respond to climate change induced environmental conditions and that this has flow on effects for their social connectivity and the social network of the group.

animal behavior and cognition↗

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. 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-{beta} 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.

evolutionary biology↗

The variability of song variability in wild and domesticated zebra finches Taeniopygia guttata

Birdsong is a classic example of a learned social behavior. Like many traits of interest, however, song production is also influenced by genetic factors and understanding the relative contributions of genetic and environmental influences remains a major research goal. In this study we take advantage of genetic variation among captive zebra finch populations to examine variation in a population-level song trait: song variability. We find that zebra finch populations differ in levels of song variability. Domesticated T. g. castanotis populations displayed higher song diversity than more recently wild-derived populations of both zebra finch subspecies T. g. castanotis and T. g. guttata, the Timor zebra finch. To determine whether these differences could have a genetic basis, we cross-fostered domesticated T. g. castanotis and Timor zebra finches to Bengalese finches Lonchura striata domestica. Following cross-fostering, domesticated T. g. castanotis maintained a higher level of song diversity than T. g. guttata. We suggest that the high song variability of domesticated zebra finches may be a consequence of reduced purifying selection acting on song traits. Intraspecific differences in the mechanisms underlying song variability therefore represent an untapped opportunity for probing the mechanisms of song learning and production.

animal behavior and cognition↗