Lead contamination increases fear and decreases take-off performance in the sparrows of Broken Hill

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The population of house sparrows in Broken Hill, New South Wales, are exposed to high levels of lead (Pb) in the environment, as a result of contamination from mining activity in the city. Over the past five years we have been looking at the effects of this lead on the population of sparrows. In a recently published paper by Dr Janet Chik, we examined the effects of lead on anti-predator behaviour and performance.

In our new study (here), we have used the gaze sensitivity test to demonstrate that sparrows with high levels of lead in their blood, are more risk averse than those in less contaminated parts of the city. The gaze sensitivity test works because sparrows have lived alongside people for thousands of years. Normally people ignore them, but sparrows have learned that when people fix their gaze on them, that normally signals danger. In the experiment we presented one of the three images below, to sparrows visiting a feeding station. When the picture of the man was looking straight at the birds, sparrows took longer to visit the feeder than when the man in the picture was looking sideways, similar to results seen previously in other urban birds like seagulls in Europe. However this result was only found in the birds that were contaminated with lead.

Figure 3 from the paper, illustrating the experimental set-up and the images used to test the sparrow’s sensitivity to possible predation.

This finding suggests that these birds were more vulnerable to predators, and therefore were more cautious. It is cool, but perhaps not surprising to see how sensitive sparrows are to the gaze of a person. That has come from adapting to the threat posed by people in the thousands of years that house sparrows have lived alongside people.

In a second experiment we tested vulnerability to predation by measuring the take-off speed of sparrows from different parts of the city. We found that birds from contaminated areas with high levels of lead in their blood, were slower to take-off in experimental trials, over the first metre of an escape flight. This difference could mean life or death when a sparrow is attacked by an ambush predator such as a sparrowhawk, and explains the sensitivity of the sparrows to the gaze of a predator.

This study is important because it demonstrates that the lead (Pb) contamination in the urban area of Broken Hill is adversely affecting the sparrows that live there. Lead is known to affect muscle strength, and cognitive behaviour in many animals. If the lead is affecting the sparrows living closely alongside people in Broken Hill, then it also suggests that the contamination through the city may pose impacts to the health of the people that live in those same areas.

Where does genetic diversity come from?

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Despite looking the same, no two zebra finches are ever alike, and that is because whenever an offspring is produced, the genetic material is a novel combination of that from it’s mother and father. In addition, novel mutations arise during the process of creating eggs and sperm, and that provides variation which selection can act on, leading to evolution of new species over millions of years.

In our recent study, led by Djivan Prentout (and the team at Columbia University, New York) we studied the whole genome sequences of 80 individual zebra finches from our captive population in Sydney. The birds came from three generations, i.e. offspring, their parents, and grand-parents. This allowed us to examine the number of mutations that arose as DNA was copied from one generation to the next.

Germline mutation and meiotic recombination are fundamental genetic processes that give rise to genetic diversity and fuel evolution. Most of our knowledge about these processes stems from a handful of model organisms and studies in mammals. Here, we characterized properties of mutation and recombination in the zebra finch (Taeniopygia castanotis), which, like other birds, differs from mammals in several potentially salient respects, including its karyotype and the mechanism by which recombination is directed to the genome. By sequencing the genomes of three-generation pedigrees, we identified de novo mutations and recombination events (both crossovers and non-crossovers).

We identified a total of 202 do novo mutations and 1088 cross-overs (whereby novel combinations of chromosomes were produced in offspring.

Our analysis indicates that the sex-averaged mutation rate is comparable to those of mammals with similar generation times. Several aspects of recombination resolutions are also similar to those in mammals, notably the estimated ratio of crossovers to non-crossovers. Thus, our findings indicate that many aspects of mutation and recombination remain conserved over large phylogenetic distances

The study can be found here

Constant companions: Zebra finch pairs are extremely close (temporally and spatially)

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In our recent paper (here), we demonstrate just how closely a male and female zebra finch move around together. The study, which was led by Chris Tyson (Wageningen University), used small solar-powered radio-tags connected to an automated sensor array, to track the movements of individual birds as they moved around in our main study site at Gap Hills. We know that zebra finches mate with a partner for life, and that they become very behaviourally coordinated over time. However, until we used this new cutting-edge technology we didn’t know just how tightly coordinated their behaviour was. Here we revealed that the distance between partners was usually about 50m, and in reality they were probably closer, because the technology was only able to localise a bird to within about 35m with great accuracy. As illustrated in the photos above, our tracking of the 32 individuals in 16 different pairs, indicated that as the birds moved around throughout the day to water, their nest, and whilst foraging, they did so very closely with their partner. This new study contributes towards our growing collection of studies that have characterised the quality and closeness of the pair-bond in the zebra finch. The pair-bond is particularly tight in this species, and probably helps them to survive and reproduce effectively in the harsh arid zone of Australia in which they live.

Parents struggle to feed their nestlings in heat waves

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In our recent paper, led by Madeleine Wheeler, we continue our examination of the effects of extreme heat on zebra finches. We have previously found that when young are raised in hot temperatures they end up being smaller as adults, and this could be explained either the direct effect of hot weather on their physiology, or perhaps on the ability of their parents to provision them with food during such hot conditions. Here we analysed nest visitation rates over a range of temperatures and demonstrated that, indeed, when temperatures became extremely hot, parents reduced the rate at which they visited nestlings. This result is consistent with our earlier findings that adults are unable to forage in such conditions (Funghi et al 2019) and that desert birds generally avoid breeding in the hottest times of the year (Englert Duursma et al 2017, 2019). The paper can be found here.

Spread of yellow-bill-color alleles favored by selection in the long-tailed finch

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It’s very exciting to see the publication today in Current Biology of our paper that describes the genomic basis of the bill colour variation in the two sub-species of the long-tailed finch. This is one of the key questions that I have been working towards with Daniel Hooper since 2015. Since our first field trip together to the Top End of Australia, Daniel has examined the genome sequence of over 1,200 individuals from across the wild range of the birds, and captive bred hybrids in the laboratory (many of which were sampled and bred by Callum McDiarmid). The cutting edge genomics has been completed with input from Peter Andolfatto, Frank Chan and Marek Kucka; the biochemistry of the carotenoids underlying the yellow and red bills was unravelled by Geoff Hill, Matthew Powers, and Nicholas Justin; and finally the work examining the fine anatomy of the retina was done by Nathan Hart, who demonstrated that even though the yellow-billed birds don’t make red carotenoids to put in their bills, they do still make them to use in the oil droplets that are used to filter light in the retina. It’s been super cool to work with all these amazing people to complete this huge study. The scale of the work can be seen in Fig 1 from the paper below that shows the sites that were sampled in the wild (E) and the variation in colour across them (F) and the lab-bred hybrids (D). The full paper can be found here

Southern Black-throated finch work

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It’s very exciting to report that Lyanne Brouwer and her team have just tagged the first southern black-throated finch up in Townsville. This endangered bird has declined across over 90% of its range in the past half century and there are only two areas in which they can be regularly found. One of these is the study site on the outskirts of Townsville.

To better manage and preserve these beautiful birds we do need to understand their habitat requirements, behaviour and movement ecology. In our project we are aiming to track birds intensively as they move around to gain important insights into these areas.

A number of birds will be fitted with these very small and lightweight radio tags. The signals will be picked up by a number of radio nodes, which will allow us to understand how much they are moving on a daily level and which areas of the local habitat they are utilising most.

The field team, led by Prof. Lyanne Brouwer, with Tis Voorstman and Parvaiz Yousef.

Mitonuclear interactions and speciation

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About a decade ago it was first proposed that the tight interaction between the nuclear genes, and the mitochondrial genes might play an important role in the process of speciation, contributing to patterns of geneflow across closely related species where they are in contact with each other. We were inspired to work in this area by Paul Sunnocks’ work on the eastern yellow robin, and Geoff Hill‘s excellent book ‘Mitonuclear Ecology.

Our first major paper testing these ideas has just been published in Molecular Ecology, and was part of Callum McDiarmid’s PhD thesis work (link to paper).

Our study was built on an amazing pre-existing knowledge of the highly conserved nuclear and mitochondrial genes that are largely shared across eukaryotes, and help to drive the operation of the mitochondria in cells, that produce most of the cellular energy. In birds 37 genes in the mitochondrial DNA (mtDNA) work closely with around 1,500 nuclear genes. This prior knowledge allowed us to characterise the differences between the two subspecies of long-tailed finch that we have been working on in the wild and laboratory for many years. The yellow-billed (acuticauda) and red-billed (hecki) subspecies last shared a common ancestor around 0.5 million years ago.

Poephila acuticauda acuticauda (the yellow-billed form from the western part of northern Australia) and Poephila acuticauda hecki (the red-billed form from the eastern part of northern Australia). (Photo Simon Griffith)

Due to the well-worked genetics of mitochondrial respiration in birds and other organisms, and the genomic sequencing that Daniel Hooper has been leading in the long-tailed finch as part of our collaboration, we were able to ascertain that there were fixed differences in just 0.9% of the sequence of the protein-coding genes between the two sub-species. There were also fixed differences in non-coding regions, that could effect the transcription, translation, or replication of mtDNA.

Figure 3 from McDiarmid et al (2024) – illustrating the evolutionary divergence for the 13 protein-coding mitochondrial genes indicating that just

An organisms mitochondrial DNA is inherited only from it’s mother, and this allowed us to generate experimental offspring in the laboratory in which the mtDNA was in the wrong nuclear genetic background. This was done by first breeding F1 hybrid offspring – produced with either a yellow mother and red father, or vice versa. In these F1 hybrids, the mtDNA matches the sex chromosome (ZZ in males and ZW in females) that was inherited along with the mitochondria from the mother. Crucially however, when we backcross female hybrid offspring to a parental type male (paternal backcross) the mitochondrial DNA end up in the ‘wrong’ genetic background.

Figure 2 from McDiarmid et al 2024 – Explaining the laboratory cross design that allowed us to place the mitochondria in the ‘wrong’ nuclear genetic background.

Using this experimental design we tested for functional effects of mitodiscordance (i.e. when mitochondrial DNA does not perfectly match nuclear DNA), using an Oroboros oxygraph machine to measure cellular respiration in cells from the different crosses. This machine can effectively measure the respiration capacity – the ability of an organism to make the cellular energy that fuels all growth, movement and cellular activity.

Our key findings were that we found a significant difference in the respiration capacity (the ability of an organism to make the cellular energy that fuels all growth, movement and cellular activity) of the two different types of mitodiscordant crosses, but not between those and other types of cross, like those between pure parental types (see the difference between Group 5 and 6 below).

The difference between these two mitodiscordant backcrosses that we have demonstrated using a careful experiment in the laboratory is entirely consistent with the pattern of admixture in the wild. Group 5 here are individuals with acuticauda mtDNA in an otherwise hecki genome, while Group 6 individuals have hecki mtDNA in an acuticauda genome. The acuticauda mitotype therefore performs relatively poorly in the wrong background, compared to the hecki mitotype. The two subspecies are in contact in the wild, and we have found that 83% of those individuals that have mismatched mtDNA and nuclear genome in the wild have the hecki mitotype (i.e. as we have shown experimentally, that mitotype performs better when in the wrong background). Secondly, in the wild the contact zone between the subspecies is slightly complicated with the cline of mtDNA displaced about 55km to the west of the nuclear DNA cline. i.e. the hecki mtDNA is able to move further westwards, presumably because it performs better than the acuticauda mitotype in the zone of mixed genomes.

Figure 1b from McDiarmid et al (2024). This clinal analysis illustrates that the mtDNA cline is displaced further to the west than the nuclear DNA cline. i.e. the eastern mitotype (hecki) does better in a western acuticauda genomic background than vice versa.

In summary, whilst there is a relatively low level divergence between the mitochondrial DNA of the two subspecies that we have been studying in northern Australia, using experimental crosses in the laboratory, coupled with a sophisticated method for measuring the efficiency of cellular respiration, we have been able to show how functional differences can effect the introgression of genes from one from into another when species come together in secondary contact. Our findings from a bird add to recent work on other animals that support the idea that interactions between the mitochondrial and nuclear genomes can play important roles in the speciation process.

Another Lundy PhD thesis

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Congratulations to Janet Chik who today submitted her thesis, entitled “The evolutionary and ecological drivers of senescence in two wild passerine systems”.

Janet completed a joint PhD between the University of Groningen (Netherlands) and Macquarie University. In Europe Janet was supervised by Prof. Hannah Dugdale and Dr. Julia Schroeder and by myself in Australia. Janet worked on the best study species – the house sparrow Passer domesticus. Janet’s research was on telomeres in the context of the long-term population of sparrows on Lundy Island, and the context of lead (Pb) contamination in Broken Hill Australia.

Janet is the most recent in a long line of students to have focused their PhD research on the sparrows of Lundy Island, including myself back in the mid-nineties.

Reproducibility of ecological data

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After twenty years of procrastination one of our bluest datasets has finally been analysed! The data was one of two sets of data used in a ‘many analysts’ study to look at how the choices that are made in an analysis pathway affects outcomes. The study is covered in a news story published today in Nature.

https://www.nature.com/articles/d41586-023-03177-1

The dataset was one of two that were analysed by 246 biologists in the study which is available online. The variation in the outcomes was remarkable given that all analysts started with the same dataset and were addressing the same question – how is nestling growth affected by the number of siblings that offspring have in the nest. There is continuous variation in the effect that analysts found. A number of analyses found significant positive effects, many found no effect and the majority found significant negative effects of siblings on growth. The study is revealing about the robustness of results in ecology and should hopefully help lead to a different approach to analyses in the future.

Congratulations to Frigg

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Frigg Speelman recently won the Macquarie University 3MT competition. The challenge of this competition is to deliver a three minute verbal presentation summarising the focus of her thesis. Frigg’s success was covered by a nice article in the Macquarie Newsletter here.

Frigg missed the award ceremony as she was in the field, catching chirupping wedgebills

THE UNEXPLORED BENEFITS OF JUST HANGING OUT IN A SOCIAL HOTSPOT

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Our attempts to understand avian behaviour usually focus on important components of life such as foraging, territorial defence, breeding and anti-predation strategies. In our study of the zebra finch, led by Hugo Loning, and a collaboration between researchers from Wageningen University (Netherlands), and Macquarie University (Australia), we focused our attention on what the birds are doing in their downtime – the bits of the day when they aren’t actively engaged in other behaviours, and are just ‘hanging out’.​ The habitat of the study site near Fowlers Gap research station is a very open grassland with small patches of acacia trees, such as those in this ephemeral creek line.

The study was conducted at Fowlers Gap Arid Zone Research Station in arid Australia where a wild population of zebra finches has been the focus of research for 19 years. We identified a number of specific trees or bushes throughout the study area that were frequented on a regular basis by groups of zebra finches. These locations, identified as ‘social hotspots’ were not obviously different from other bushes or trees in the same area, either structurally, or in their position. However, they were the focus of prolonged social gatherings over the course of the study, and anecdotally some had been in use consistently for several years. The social hotspots were identified both by the frequent presence of zebra finches in them, but also by a significant accumulation of zebra finch droppings underneath them. One of the social hotspots was found in the dead tree to the left of this picture. Social hotspots were found in both living and dead trees, and they didn’t differ in an obvious way from other trees or bushes in the local vicinity. Large accumulations of droppings were found underneath social hotspots, indicating their prolonged use by large numbers of birds.

In our study, we characterised social hotspots using direct observational work and longer-term acoustic monitoring. The social dynamics of the hangouts were quite complex, with birds typically arriving and departing in smaller groups, rather than all in a single group. Social gatherings could collectively last for hours at a time, even though individuals came and went, and probably few were present for the whole duration of the hangout.

There were birds present in these social hotspots for over 35% of the hours of daylight, and consequently, these specific locations provided individuals with a good opportunity to find and meet conspecifics from the local population. Although zebra finches usually moved around the local area in pairs, or small groups, the social hangouts were occupied by an average of about 30 birds, with as many as 77 birds hanging out together in a typical acacia tree about 3m wide and 3m tall. The social hotspots therefore provided lots of opportunity for social interactions with many birds from the local population, and there was typically a consistent level of vocalisations, including lots of singing, by multiple males.

Although our study was unable to follow individual movements or participation in these social gatherings, we suggest that social hotspots and hangouts such as those that we have described in the zebra finch are an important, and often neglected part of social behaviour in birds. They will provide a relatively safe refuge during the day where individuals can take advantage of safety in numbers, whilst resting, preening, and socialising with conspecifics.

Further study of such social hotspots should provide insight into their capacity to increase social networking opportunities and information exchange across the wider population. We believe that social hotspots and hangouts are a neglected feature of the behavioural ecology of many social birds and are worthy of further attention.

Tracking sperm and testosterone over reproductive stages in the zebra finch

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Sometimes it takes a while to get studies out….. Finally this week our paper describing the variation in sperm and testosterone over the breeding cycle was published in Hormones and Behaviour. The study was initiated back in 2011 through discussions between Kate Buchanan, Melissah Rowe and myself. The study was supported by funds from the Australian Research Council awarded in 2012 and then conducted by Lori Hurley as part of her PhD. Two postdocs, Ondi Crino and Riccardo Ton have also made significant contributions to the study, by dealing with a complicated dataset and writing the manuscript.

The study characterises variation in the level of testosterone circulating in the blood of males across different stages of the breeding cycle (nesting, egg-laying period, incubation, and nestling rearing), and how those levels covary with the morphology and motility of sperm. This contributes useful knowledge to our understanding of how birds that breed opportunistically (whenever conditions are suitable) manage trade-offs between different physiological traits. Whilst many birds have a very seasonal pattern of breeding, with a flush of hormones and production of sperm arriving with the lengthening days of spring, zebra finches remain reproductively active throughout the year. In the desert, conditions can be suitable for breeding throughout the whole year, depending on when the rain falls.

We showed that testosterone levels were fairly low across different breeding stages, but did significantly increase at the time when a males’ partner is about to become fertile again (as one set of offspring are about to fledge. The higher level of testosterone makes sense, because we demonstrated that higher testosterone is related to the swimming performance of sperm.

Fig 4. From Hurley et al (2023). The relationship between sperm swimming speed and the testosterone level in his blood (A) and his body condition (B).