White Gum’s and Whites’ Skinks; disentangling climatic effects on manna quality and lizard mating behaviour

By Zach Borthwick, Amy Wing and Geoff While

May 23, 2020

Zach and Amy finished up their honours this week following a covid interrupted 9-month research project. Zach and Amy undertook very different projects that focussed on two key areas of the BEER groups research interest. Both executed their honours projects with great dedication and their findings are going to lead to some significant outputs as well as hopefully set the stage for a bunch of neat research moving forward.

Zach’s project examined how changes in the thermal environment mediates the opportunities and targets of sexual selection and the mechanisms underpinning these effects. This question is of fundamental importance, as sexual selection is increasingly recognised as an important predictor or population viability. Rising temperatures have the potential to alter the opportunity, strength and targets of sexual selection via a number of different mechanisms. These effects range from shifting the availability of viable gametes to impairing fecundity as well as skewing operational sex ratios in species with temperature-dependent sex determination. However, perhaps the most influential effect of temperature is that it will impose physiological constraints on energetically demanding behaviours, which includes mating activities.

A pair of Liopholis whitii skinks.

Zach’s honours project tested this. Zach, under the supervision of Jen Moss, executed a huge experiment whereby he manipulated the thermal environment of semi-natural populations of Liopholis whitii during the mating season, creating a sun and a shade treatment. He collected detailed data on male and female activity and used this to assess how the thermal environment mediated male and female encounter rates. Following birth, Zach generated paternity data from the resultant offspring which allowed him to examine the consequences of behavioural responses to the thermal environment for reproductive success and ultimately patterns of sexual selection.

One of the shade enclosures at our large Cambridge farm facility set up and ready for lizards.

Zach found several interesting results. First, Zach found strong differences in activity between the treatments. Specifically, where lizards were usually more active in the sun treatment, when days were really warm, lizards in the shade treatment would make the most of the increased thermal opportunities and really ramp up their activity, beyond that of lizards in the sun treatment. This created hugely dynamic patterns of activity across the duration of the experiment that were tightly linked to daily temperature, but in treatment specific ways. Activity was a significant predictor of home range overlap, with more active individuals having greater overlap with the opposite sex than less active individuals. As a result, there was some evidence that individuals in the sun treatment had a greater proportion of their home range overlapped by members of the opposite sex than individuals in the shade. There were also strong differences between treatments in reproductive success. The most striking was that females in the shade treatment had lower reproductive output than those in the sun. This was driven by less females reproducing overall in the shade treatment rather that differences in reproductive output between the treatments. The reason for this is still the subject of investigation, but it resulted in a significant shift in the operational sex ratio. In line with this, we found some evidence for shifts in the opportunity for sexual selection between treatments – with standardised variance in male reproductive success greater in the shade vs the sun treatment. We also found evidence that treatment influenced the targets of sexual selection, with strong selection on male body size in the sun enclosure but not in the shade treatment. Combined, Zach’s results point to the significant roll that the thermal environment can have on patterns on reproductive behaviour and success, a role which has the potential have downstream consequences for the ecological and evolutionary trajectory of populations.

A Pardalote deciding which White Gum it is going to “farm” for manna.

Amy tackled an altogether different research question. Amy’s project, co-supervised by Julianne O’Reilly-Wapstra and Peter Harrison, was focused on trying to understand what mediates variation in White Gum manna. White Gum manna is a key component of the diet of the endangered Forty Spotted Pardalote. Importantly, our previous research has shown that, within a population, White Gums vary considerably in the quality of manna and that Pardalotes prefer trees that have manna that have lots of good sugars (e.g., sucrose) and little indigestible sugar (e.g., fructose). However, we currently have no idea what underpins this variation in manna quality. Addressing this question is crucial if we are to understand what drives Pardalote distributions at both a micro and a macro scale. It will also provide important information when making decisions about how to restore key Pardalote habitat.

A hard day sampling White Gums for Manna – this time at Inala Nature Reserve

To address her research question, Amy took a two-pronged approach. First, she utilised an established common garden trial, in which White Gums from multiple different populations (spanning the climatic distribution of the species in Tasmania) were planted in two different environments. Second, she collected samples from white gum populations spread across Bruny Island, the stronghold of the Forty Spotted Pardalote. In each of these contexts, Amy extracted Manna for trees and quantified the sugar content using Liquid Chromatography Mass Spectrometry. Amy found that, on Bruny, there was huge variation in manna composition between trees from different populations, underpinned primarily by variation in sucrose and raffinose. This variation was closely linked to aridity gradients across populations, with populations of trees with a greater proportion of sucrose (tasty trees) found where aridity was highest. The common garden trial was designed to explicitly disentangle the contribution of genes vs environment in mediating this variation in manna. In contrast to Bruny, Amy found no difference between common gardens in the extent of manna quality nor did she find a strong signal for a genetic effect, that is there was no consistent variation between trees from the different source populations. However, the number of trees from which manna was successfully extracted was limited in these trials, potentially constraining our ability to tease apart relatively subtle effects of genes or the environment. Hopefully more manna can be collected in the future to address this.

Bruny island – one of the last strong-holds for Forty Spotted Pardalotes.

Overall, Amy’s research provided a tantalising glimpse into what drives variation in manna quality across the White Gums range. This provides the foundation for a range of future research projects that designed to tease apart the relationship between climate, manna, and the Forty Spotted Pardalote. Specifically, more detailed sampling inside and outside the Pardalote range to ask whether manna quality is a predictor of the Forty Spotted Pardalote across Bruny, more detailed experimental approaches that allow us to understand the mechanisms linking this potential association between aridity and manna quality, and modelling approaches that allow us to ask how changes in aridity as a result of our changing environment, may shift the quality of this fundamental resource. Exciting times ahead.

Dire times ahead for Tasmania’s alpine specialists

By Heather Bryan

Dec 20, 2018

Predicting how climate change will impact species and biodiversity is a complicated task. Most methods rely on finding a relationship between species occurrence records (locations where a species has been recorded historically) and climatic variables, then using this relationship to predict future locations, given expected changed climatic conditions. However, this method ignores the mechanisms restricting or allowing species distributions and does not account for demographic processes that dictate species occurrence. Heather’s honours project addressed this shortcoming by coupling species distribution models with long-term demographic data to predict the distribution and population dynamics of four species of snow skink; two lowland species (Niveoscincus ocellatus, N. metallicus) and two species currently restricted to highland areas (N. microlepidotus, N. greeni).

Tasmania’s unique snow skinks; Niveoscincus metallicus (top left), N. ocellatus (top right), N.greeni (bottom left), and N.microlepidotus (bottom right)

Heather’s data suggests hugely divergent predictions regarding the consequences of climate change for lowland and highland snow skinks species. Lowland species are predicted to significantly expand their range in the future. This will be a function of both an increase in suitable habitat at higher elevations and the maintenance of suitable habitat in low elevations. This means that this species will be able to move into higher and higher elevations while still maintaining their lowland distribution. This increase in range size also corresponded with an increase in population abundance, suggesting an overall positive impact of climate change for the lowland species. The story is not quite so rosy for highland species currently restricted to alpine areas. In contrast to the lowland species, these species are predicted to experience significant contractions in their suitable habitat, being restricted to higher and higher elevations. Indeed, the highland species are predicted to reduce their distribution by up to 93% of their current range. What is even more worrying is that the predicted reduction in population abundance was even higher at 98%! This suggests the imminent decline and potential extinction of these unique highland lizards within the next century. Such patterns are consistent with other range-restricted specialists many of which are predicted to show similar decreases in distribution and abundance with climate change.

Changes in distribution of the two highland snow skink species, N. microlepidotus (a – c) and N. greeni (d – f),  over the next 65 years.

So why are these highland species so vulnerable to climate change? Alpine and widespread snow skink distributions currently overlap at a narrow thermal band, usually occurring at approximately 1100 metres above sea level.  Such congeneric range separation is often indicative of interspecific competitive interactions. This is exacerbated by the fact that highland species have a unique biennial reproductive cycle, which limits reproductive output to once every second year compared to their lowland counterparts which give birth annually. Consequently, the restriction of alpine species into the future will most likely be mediated by increased competition from lowland species that are moving up the mountain and taking over all the suitable habitat. Heather’s models provided some early evidence that interspecific competition will indeed influence predictions. Specifically, Heather showed that the predicted shrinking of habitat for highland species was reinforced by a predicted upslope shift in the competitive band. The next step will be to incorporate such competition more explicitly into these models and ultimately give a more precise estimation of how and where competition occurs, and how climate mediates interspecific interactions.

Combined Heather’s data provides compelling evidence that snow skinks will be affected by climate change and that highland species may become extinct by 2085. This begs the question what should and can be done about this. There is no simple answer. On the one hand, replacing a small alpine snow skink with a small lowland snow skink may not have any meaningfully functional effect on the ecosystem. Thus, perhaps intervention is unwarranted. On the other hand, the highland snow skinks represent one of only a small number of alpine lizard specialists globally, and thus their disappearance would constitute the loss of a unique component of our biota. There are several ways in which this could be mitigated. The first is via in situ protection of suitable habitat. However, as the alpine areas that these species currently persist represent some of the best protected areas in Tasmania –increased protection of suitable habitat at a regional scale may not actually be possible. Therefore, ex situ conservation measures may be the only option. This could involve the translocation of alpine species to more suitable habitat. Because snow skinks already live in the coldest areas of Tasmania, translocations to mainland Australia may be required which brings with it its own significant challenges. Clearly, we are a long-way from implementing any of these measures and whatever measure we do implement will require careful consideration of the risks of decline, the technical feasibility of the approach as well as their biological risks and the socioeconomic costs and constraints. One thing that is for sure though is that whatever decision and discussions need to be had about the potential future of these unique lizards, they need to be had soon because the clock is ticking…

Eco-Evolutionary dynamics book review

By Geoff While

Dec 4, 2018

Traditionally, ecologists have primarily been concerned with population processes acting at time scales that seemed unlikely to require evolutionary considerations. Similarly, evolutionary biologists frequently dismissed the role of environmentally induced variation in traits since such effects were considered to be transient in the absence of genetic inheritance. However, there has been a growing concern that ignoring evolutionary processes limits our ability to understand population responses at ecological time scales and, conversely, that ignoring these ecological processes can lead to erroneous evolutionary inferences. Thus, one of the contemporary challenges for evolutionary ecologists is to bridge this gap and explore the links between short-term phenotypic change, population and community dynamics, and long-term evolution.

Eco-Evolutionary Dynamics is the field that has emerged out of a growing need to address this challenge. While one could argue that a focus on the dynamic relationship between ecology and evolution has a long history, the field of eco-evolutionary dynamics as we know it today has only emerged in the last decade or so. This makes Andrew Hendry’s new book, Eco-Evolutionary Dynamics, a timely contribution. Hendry is pioneer in the field of Eco-Evolutionary dynamics having authored many of the key recent reviews on the topic as well as contributed a substantial empirical body of work. He is, thus, well placed to provide an overview of where we stand and how we should move forward.

The book is split up into several sections. The first section introduces the concept of eco-evolutionary dynamics and provides a road map for the rest of the book. The second section deals the eco-to-evo component of the process – how ecological change influences evolutionary change. As Hendry points out, this amounts to a “review and recasting of the classic field of evolutionary ecology”, transitioning from selection, to adaptation, to divergence and finally speciation. The third section deals with the evo-to-eco component of the process – how short-term evolutionary change can impact population dynamics, community composition and ultimately ecosystem processes. These represent the more under-explored areas of eco-evolutionary dynamics and will provide the uninitiated reader with several novel insights into the field. The fourth section deals with the underpinnings of these effects, focussing first on genes and genomes and then on plasticity. The final section wraps things up providing a summary of what we do and don’t know about eco-evolutionary dynamics and articulates several areas for future research.

There is a lot to like about this book. Hendry strikes a nice balance between explaining detailed eco-evolutionary concepts in a simple manner with an extremely wide range of literature that provides context to those concepts. Hendry focuses on the importance of studying phenotypes in natural settings but also draws substantially from the wide range of work undertaken in controlled laboratory studies. In doing so, he doesn’t pretend to explain everything but instead highlights key areas of the process for which there is currently conflicting evidence and thus areas that are ripe for further empirical scrutiny. The book is also nicely balanced in its appeal. It provides a wonderful introduction to many aspects of evolutionary ecology that will be appealing to any undergraduate or PhD student while also being detailed and novel enough to provide valuable insights and ideas for initiated readers.

There were, however, several areas of the book where I believe Hendry missed a trick. This is perhaps inevitable when trying to cover such a vast topic in one book. One was in the dealing of phenotypic plasticity. It appeared, in places, that Hendry felt a need to repeatedly justify the inclusion of plasticity in this framework. As a result, the section on plasticity was largely focussed on explaining what plasticity is rather than detailing the role it might play in mediating eco-evolutionary dynamics more broadly. This is surprising given that plasticity has arguably the greatest potential to drastically and rapidly alter the organism-environment relationship and thus shape eco-evolutionary dynamics. There was also a lack of a focus on the dynamic component of the term. While eco-to-evo and evo-to-eco received considerable attention, far less was paid to the fact that ultimately eco-evolutionary dynamics are about feedbacks between the two; from ecology to evolution and back again. Hendry acknowledges this of course, but a chapter dedicated to how these processes might come together would have helped tie the book together.

Because of the above I couldn’t help wanting more out of this book. This is not a reflection on the book itself but rather the fact that there is a fundamental lack of systems out there that are currently suitably-well understood to characterise these processes in a holistic manner. As a consequence, we are left with pieces of the puzzle rather than the completed puzzle itself. Hendry does a great job of highlighting those pieces and suggesting how they may come together but is ultimately limited in how far he can go putting the puzzle together. To his credit, he does not try to force his own agenda in this context but instead encourages the reader to take the next steps in completing the puzzle. This is no easy task. It will require designing holistic research programs, targeting natural systems that allow us to understand the dynamic nature of the organism-environment-evolution relationship at multiple levels of biological organisation. Such a goal necessitates a multidisciplinary approach that will foster collaborations between ecologists, evolutionary biologists, mathematicians, molecular biologists, developmental biologists, and many more. An integrated approach with such a broad aim should be hugely attractive to the next generation of scientists and this book will provide an excellent basis from which that generation can tackle some truly exciting new research questions. After all, who doesn’t like completing a puzzle?


Burrows and Birthing Aysnchrony – two exciting new directions for the Egernia system

By Geoff While, Deirdre Merry and Barnaby Freeman

Nov 12, 2018

Deirdre and Barnaby finished up their honours this week. This is a huge undertaking, involving 9 months of data collection, collation and synthesis. Deirdre and Barnaby’s projects tackled very different questions but had one thing in common – they both have the potential to form the foundation for two exciting new research directions for the Egernia system.

Deirdre’s project examined the mechanisms underpinning birthing asynchrony. This was carried out in collaboration with close BEER group collaborator Camilla Whittington from the University of Sydney. Birthing asynchrony is a neat trick that several Egernia species have by which they give birth to offspring over an extended period of time (sometimes up to 10 days). The benefit of this behaviour appears to be that it allows females to manipulate the competitive environment of their brood and this in turn may influence family dynamics – although this is unresolved. Interestingly, unlike other asynchronous production of offspring (think egg laying in birds) in the Egernia this happens even though all offspring are fully developed and waiting to pop out. What is even more intriguing is that females can delay the birth of different offspring within the same uteri. That is give birth to one offspring, wait, and then give birth to another offspring from the same uteri!. How females achieve this is a mystery but could give us fundamental insights into the process of live birth itself.

Deirdre’s project took the first tentative steps in unravelling this mystery. She focused on examining differences between uteri (which are independent in lizards) in how they respond to arginine vasotocin (AVT) – the key hormone that mediates the birthing process in reptiles. To test this Deirdre carried out highly sophisticated contraction assays (see below photo…) to examine the response of uteri to increasing concentrations of AVT. She combined this with molecular techniques that allowed her to evaluate gene expression for an AVT receptor, AVPR1A. Deidre found that one uterus was indeed more responsive to AVT than the other both in terms of its contraction response to AVT and in the expression levels of the AVPR1A receptor. She also found that the number of embryos in a uterus had significant effects on uterine contractile response to AVT. This suggests that pregnant female Egernia have an internal mechanism that allows them to give birth asynchronously and that developing embryos may be influential in facilitating this. Importantly, Deirdre’s honours work is just the tip of the iceberg. We need to know more about how females achieve this asynchronous birth not only between uteri but also within a uteri and also how these mechanisms may have been co-opted to function across other members of the Egernia group. So much more to find out…

How many scientists does it take to carry out a contraction assay…

Barnaby’s project examined a different trait of the Egernia, their burrow. Burrows are a type of extended phenotype, which is a trait that extends beyond that individuals physical being. Sounds complicated! But there are many examples of relatively simple extended phenotypes in nature – think about a beaver’s dam, a wombats burrow or a birds nest. Importantly, these extended phenotypes can have fundamental impacts on the environment and also influence key evolutionary processes (this is known as niche construction). Extended phenotypes are often easier to measure and quantify than actual phenotypic traits (especially behaviour) making them great candidates to ask questions about the causes and consequences of such traits. The first step in understanding such extended phenotypes is getting a handle on the extent to which they vary within and between individuals.

Barnaby’s honours project aimed to do exactly this. Egernia lizards rely on deep and complex burrow systems; they provide shelter for family members as well as access to resources. Despite this we know nothing about how individuals go about constructing these burrows. Barnaby’s project consisted of several integrated components. First, he quantified variation in burrow construction within a population of Liopholis whiti, by bringing animals into the lab and allowing them to burrow in specifically designed burrowing chambers. Second, he examined what habitat characteristics influenced where an individual burrowed in the wild. Barnaby found there was considerable variation in burrowing behaviour both between individuals (see below photo) and also within individuals across time. This variation in burrow construction was not related to morphology or sex. Finally Barnaby found that Egernia tend to occupy burrows with very specific habitat characteristics in the wild. As with Deirdre’s work, this will form the foundation from which a broader range of research can be undertaken on burrow construction. Importantly, as burrowing complexity has strong links to both morphological and social evolution in this group, this should provide the foundation from which a wide range of work can be undertaken to examine the consequences of burrowing complexity for broad scale macro-evolutionary processes.

Constructed in four weeks – Kevin McCloud eat your heart out!


Everything you need to know about Thermal Developmental Plasticity in reptiles!

By Geoff While, Lu Fitzpartick, George Cunningham and Erik Wapstra

May 30, 2018

The environment influences organisms in a myriad of diverse ways. One of the most pervasive ways that this occurs is through effects on an organism’s development during the early stages of life. Evidence for such “developmental plasticity” comes from a range of organisms, from plants to humans, from ants to elephants, and emerges across a myriad of traits, from cognition to birth date, from sex to sprint speed. Through these effects developmental plasticity has been shown to fundamentally mediate key evolutionary and ecological processes.

Reptiles have been particularly well studied in this context. Perhaps unsurprisingly, the aspect of the developmental environment that has been focused on the most is temperature (termed ‘thermal developmental plasticity’). Indeed, there is a large and growing body of work that has tested the effects of the thermal environment during development on a range of traits across all the major reptile groups. To celebrate this body of work an upcoming issue of the Journal of Experimental Zoology, Part A, will be dedicated to this topic. This issue, edited by Dan Warner, Wei-Gu Du and Arthur Georges, aims to provide a comprehensive overview of all aspects of thermal developmental plasticity in reptiles with the aim of both synthesising the literature, focusing on the major current themes, and providing a framework for moving the field forward. The BEER group was lucky enough to be asked to contribute several papers to this theme issue. Each paper tackles a different component of this overall research space and, we hope, provides an impetus for research in the future.

The opening paper, led by Geoff and Dan Noble at UNSW, focuses on synthesising the literature on thermal developmental plasticity. To achieve this we reviewed research into thermal developmental plasticity across reptiles with a specific focus on the key papers and findings that have shaped the field over the past 50 years. We then introduced a large database of experimental studies examining thermal developmental plasticity (the RepDevo database – more on that shortly…) which we use to provide a qualitative overview of the key research themes associated with thermal developmental plasticity. Finally, we suggest ways that future progress in this field can be made through targeted empirical, meta-analytic, and comparative work. Specifically, we focus on four key areas that we believe will represent specifically rewarding avenues of research. These relate to the mechanisms underpinning thermal developmental plasticity, the fitness consequences of developmental responses to temperature, macro-ecological patterns of thermal developmental plasticity and how these three play out in the specific context of sex determination. Our two empirical papers in the theme issue tackled a number of these topics specifically.

Phylogeny of the 140 egg-laying reptile taxa for which data has been collected on thermal developmental plasticity.

The first of these papers, headed up by Nathalie in Lund, focused on the underlying mechanisms that generate different developmental outcomes in response to the thermal environment. Specifically, we incubated embryos at benign and stressfully low incubation temperatures and examined how these thermal treatments influence patterns of gene expression. We show that almost 50% of all transcripts exhibited significant expression differences between the two incubation temperatures. Transcripts with the most extreme changes in expression profiles were associated with transcriptional and translational regulation and chromatin remodelling, suggesting possible epigenetic mechanisms underlying acclimation of early embryos to cool temperature. We argue that studies that combine experiments of developmental thermal plasticity with an examination of their underlying molecular mechanisms have a crucial role to play in our ongoing attempt to understand how populations adapt to thermal stress (see Nathalie’s paper in Evolution earlier this year for an example of this).

Differences in gene expression levels between thermal treatments, lineage (Italian vs French) and populations Major differences are seen between incubation temperatures (cool in blue, and warm in orange).

The second of these empirical papers focused on the adaptive significance of the phenotypic variation produced by the thermal environment during development. This paper, led by George and Lu, experimentally manipulated the thermal conditions experienced by live bearing female snow skinks. Live bearing species provide a particularly interesting test case for thermal developmental plasticity because, unlike egg laying species, they have the capacity to buffer extreme conditions via their basking behaviour. We focused on a high-altitude population of snow skinks in order to examine the consequences of thermal conditions at the range margins of a species distribution. We show that thermal conditions during development have strong effects on a number of key phenotypic traits, such as birth date, that have consequences for fitness related traits. Specifically, we found that offspring born earlier as a result of high temperatures during gestation had increased growth over the first winter of life. These results have broader macro-ecological implications as they suggest that advancing birth dates that result from warming climates may, at least initially, have positive effects in this population via increased growth.

Relationship between offspring snout-vent-length following winter and birth date in offspring from a highland population of Niveoscincus ocellatus. Data is from the field (green) and two basking treatments (4‐hr: blue, 10‐hr: red).

These papers are really just the tip of the iceberg with many other contributions to the theme issue by world leaders in this field promising to make this one of the most comprehensive and wide ranging examinations of thermal developmental plasticity to date. We were honoured to be able to make a small contribution to this pursuit and hope that our research, and that of our colleagues, promotes a new wave of interest in exploring the multifaceted nature of thermal developmental plasticity and its ecological and evolutionary consequences. Please see below for links to each of the paper and check out the theme issue when it comes on line!

While, G.M., Noble, D.W.A., Uller, T., Warner, D.A., Riley, J.E., Du, W.G. and Schwanz, L.E. (In press) Patterns of developmental plasticity in response to the thermal incubation environment in reptilesJournal of Experimental Zoology, Part A.

Feiner, N., Rago, A., While, G.M. and Uller, T. (In press) Developmental plasticity in reptiles: Insights from temperature-dependent gene expression in wall lizardsJournal of Experimental Zoology, Part A.

Cunningham, G.D., Fitzpatrick, L.J., While, G.M. and Wapstra, E. (In press) Plastic rates of development and the effect of thermal extremes on offspring fitness in a cold-climate viviparous lizardJournal of Experimental Zoology, Part A.

A social lizard pilgrimage

By Geoff While

Oct 20, 2017

Type the word pilgrimage into google and you get images of the holy cities of Mecca, Lumbini, Bethlehem and Kumbh Mela. What you rarely get is an image of Bundey Bore, a rural homestead on the outskirts of Burra, 2 hours north of Adelaide. However, for any herpetologist studying social behaviour and its evolution, this is a site of great importance. For it is at Bundey Bore, 35 years ago, that Mike Bull began his seminal work on the life of the Sleepy Lizard. This work focused initially on Mike’s interest in parasites and the Sleepys were simply a vehicle through which Mike could study host-parasite interactions. However, over the course of his days travelling the dirt roads (along with long-term collaborator Dale Buzzacott) he made several significant observations that would shape the way that we view lizards as social creatures. Specifically, Mike noticed multiple instances, up and down the roads, where two individual lizards would be found basking together – a male and a female. Indeed, the same pairs were often seen together over the full duration of the 2 month mating season. What was more surprising was that the same pairs (up to 79% of them) would also appear together the following year. We now know that some of these pairs have been together for 27 years! This initial finding, published in Behavioral Ecology and Sociobiology in 1988, was the first documented evidence of long-term social monogamy in a lizard system and paved the way for all the subsequent research on complex social behaviour in lizards that underpins much of what we do today.

Classic Sleepy Lizard habitat – salt bush desert.

I was fortunate enough to make this pilgrimage during a recent trip to South Australia. As many of you know, Mike unfortunately passed away late last year, but his legacy continues on through the work of his students as well as Mike Gardner, Mark Hutchinson and Andy Sih, three collaborators who Mike had worked closely with over many years. I was out there with Andy’s research group, which comprised of BEER group alumni David Sinn as well as Orr Spiegel and PhD student Eric Payne. Andy, Orr and David have been working at a specific part of the site for the past 5 years where a marked population of Sleepys live. The Sleepy’s are caught early each season and fitted with radio collars and then tracked for several months to determine home range locations and also their favourite sleeping bushes. As I found out, tracking Sleepy’s is not as easy as it would seem – these are swift creatures that zip between bushes meaning that the only way that you can wrangle them is from the side of a moving vehicle… Only joking – each and every one of the sleepy lizards I tracked was curled up under a bush like a kitten taking a nap… During the field season, lizards are re-caught and behavioural assayed several times as well as assessed for parasite prevalence. The focus of Andy’s  group, building on substantial previous work by Stephan Leu and Steph Godfrey, is primarily on tracking the movement of several strains of ticks introduced into the population and understanding how an individual’s behavioural type and their position within the social network mediates the movement of parasites between individuals. All in all, it was great to see how the site works, to wrangle some Sleepy’s and to see Mikes work continue.

I caught one of these two creatures while it was curled up under a salt bush having a nap – I will let you guess which one…

The main reason for being in South Australia, however, was to attend a symposium celebrating Mike’s life and, specifically, his recent achievement of having his 300th paper accepted. The symposium, thoughtfully and thoroughly organised by Mike Gardner, was divided into the four main themes of Mikes research – lizard social behaviour, social network analysis, the importance of long-term data sets, and, of course, host-parasite interactions. There was a fantastic range of talks from Mike’s students and collaborators as well as fantastic plenaries from Andy, Steph and Corey Bradshaw, which helped provide context for Mike’s significant contribution to those fields. The symposium was excellently attended and it was really nice to meet and interact with some of Mike’s family and convey to them, hopefully, the impact that Mikes work has had on what we do. For those of you interested I believe there is a link to a video of the talks here (http://video.flinders.edu.au/events/Mike_Bull_Symposium_2017.cfm) and there will be a special issue of Austral Ecology celebrating Mikes work coming out in due course.

Mining the good stuff: foraging behaviour in an endangered Pardalote

By Inala Swart and Geoff While

May 23, 2017

The behaviour of individual animals can have substantial implications for the structure and function of whole communities and ecosystems. A classic example of this is the beaver which, through its dam building behaviour, can alter whole landscapes and subsequently the community of organisms that live in those landscapes. Animals, such as the beaver, that cause wide scale changes in the landscape are obvious candidates to study the implications of their behaviours at higher levels of biological organisation (populations, communities, ecosystems). However, many other species alter their environment in much more subtle ways that never-the-less can have substantial impacts on the potential makeup of the community around them.

Forty-spotted pardalote at Inala, Bruny Island

One potential example of this is the Forty-spotted pardalote (Pardalotus quadragintusi), a small endangered Tasmanian bird. Forty spotted pardalotes forage for a critical food resource known as manna. Manna is a sugary exudate from Eucalypt trees. Manna is acquired by the pardalotes through ‘mining’ whereby adult birds create small incisions in the stem surface promoting the flow of manna. Indeed, Forty-spotted pardalotes have a specialised beak for undertaking this task. Only white gums (E. viminalis) produce manna to any significant degree and the manna from these trees makes up >80% of the food provided by Forty-spotted Pardalote parents to their nestlings. As such the Forty-spotted pardalotes are reliant on white gum habitat. Importantly, manna is also an important food resource for many other woodland species, such as a range of insects, arboreal mammals as well as other woodland birds, and the behaviour of foraging pardalotes strongly influences the availability of manna. Therefore, Forty-spotted pardalotes have the potential to act as ecosystem engineers; playing a fundamental role in the availability of manna in the environment and consequently the occurrence and abundance of other manna dependent species within the community. However, we currently know almost nothing about what influences the mining behaviour of these unique birds.

Inalas honours project focused on whether pardalotes had preferences for certain white gums within their territory and whether variation in tree characteristics or manna quality influenced the tree use of the pardalotes. This involved behavioural observations; watching the pardalotes as they fed in the white gums and recording the proportion of time they spent in each tree per territory. Inala found that Forty-spotted pardalotes tended to use one particular (primary) tree within their territory, often spending more than 80% of their foraging time in those particular trees. Inala then collected detailed information on the characteristics of those primary trees so that she could compare differences in tree characteristics between primary trees with the other trees in the pardalotes territory. Specifically, Inala measured a number of traits for all those trees and collected manna from them, by replicating the pardalote’s action and incising stems and branches. The manna Inala collected was then analysed at UTAS’ Central Science Laboratory, where the types and relative amounts of each sugar present in the manna was quantified.

So what did Inala find? Inala found that the primary trees were often larger, closer to the nest site, and further from their nearest neighbours than trees that were used less or not at all by the birds. This is perhaps intuitive and consistent with a number of studies, which have demonstrated the importance of large hollow bearing trees for pardalotes to feed and nest in. However, Inala also found that manna composition played an key role in pardalote tree use. Inala found that the manna was composed of over 20 different types of sugars, many of which have not been identified in Eucalypts previously.  However, two major sugars dominated the manna composition; sucrose, which provides a valuable energy source for the pardalotes, and raffinose, which is largely indigestible. These two sugars were negatively correlated with one another, so that trees with high amounts of sucrose had low levels of raffinose and vice versa. Interestingly, Inala found that the pardalotes primary used trees that had manna with far higher ratios of sucrose to raffinose, suggesting the pardalotes were selecting trees based on the quality of their manna.

Understanding what characteristics pardalotes depend on in their habitat is important both in understanding how their behaviour may shape inter-specific interactions as well as for practical conservation applications. As detailed above, many species depend on manna as a food resource, but none are known to be able to actively procure it from white gums in the same way as forty-spotted pardalotes can. Pardalotes may therefore be the agent by which ‘genes-to-ecosystems’ effects of white gums, a dominant species in these woodlands, may flow on to the rest of the community. This could lead to interesting questions regarding competition between pardalotes and other birds, as this is already known to be a threat facing pardalotes. Understanding what pardalotes prefer in a food resource is also important for conservation. It provides better understanding of why pardalotes may depend on certain trees, and provides groundwork for long term management goals such as selecting appropriate seedstock for re-vegetation or even formulating artificial diets should captive insurance populations ever need to be established. All these questions represent exciting avenues for future research and we encourage any one who is interesting in exploring some of these themes to contact us.

Indiana Yang and the Origin of the Tuscans

By Tobias Uller and Geoff While

Apr 26, 2017

This year marked the 6th in our quest for the evolutionary origin and introgressive spread of a sexually selected syndrome in wall lizards. It marked a return to central Italy to fill in the remaining gaps in the map tracing the origins of this phenotype. What has been revealed so far is an intricate history of isolation, evolution, and conquest through interbreeding.

Here is the background to the Italian drama. The ancestral phenotype of the wall lizards is characterised by brown coloration and relatively small body size. This phenotype persists across the wall lizard’s current distribution, from western Spain throughout most of southern Europe and into the eastern Greek islands. However, in the not-so-distant past a population of wall lizards somewhere on the west coast of Italy evolved a suite of highly exaggerated characters – larger heads, bulkier bodies, green-and-black colour, aggressive behaviour, to name just some features. The green-and-black lizards – we call them Tuscans, but they are formally described as P. muralis nigriventris – later came into contact with their closest relatives, and then with a much older lineage evolving in western Europe. Both of these retain the usual brown wall lizard phenotype. Since then the whole suite of characters has spread via introgressive hybridization to cover most of the lowland areas from south of Rome to Genoa in the West, Bologna and Modena in the North, and the Appennines in the East.

Phenotypes of the sampled populations in Italy vary from “Tuscan” (green) to ancestral (brown)

The first aim of our research has been to reveal when and where this all happened. This detective work has so far taken in 100+ wall lizard populations in Italy. Like any good detective story, our suspect for the location of the origin of the Tuscan phenotype has been a moving target, constantly changing as more phenotypic and genetic sampling has ruled out potential hypotheses and given rise to others. This year saw the final pieces of the puzzle come together and, thanks to Yang and Hanna’s efforts in the lab, we expect to release a detailed evolutionary history in due time.

Tobias and Yang catching Lizards

The second aim is to nail down who is guilty. We know one part of the answer: sexual selection. The exaggerated characters give males an advantage in competition with other males. Male-male competition thus promoted the evolution of the green-black phenotype during their time in geographic isolation. Sexual selection is also what has made the suite of characters introgress as the lizards came into contact with lizards of different genetic lineages. What remains to be understood are the ecological conditions that made sexual selection take off and persist to drive the characters to fixation.

None of the introgressive spread would be possible, however, unless genomic and developmental organisation allowed the transfer of a whole suite of characters between lineages. Despite that the characters are quantitative, their spread is associated with limited overall genetic exchange. Thus, evolution of this suite of characters is shaped by, and probably shapes, genomic and developmental modularity. We suspect that an ancestral developmental organisation may contribute to the repeated evolution of similar phenotypes across wall lizard species. This is exciting because theoretical studies (Jones et al. 2014; Watson et al. 2014) suggest that evolution of development under correlational selection can make even random mutation produce phenotypes that are non-random with respect to fitness. One of our main long-term goals is therefore to use the wall lizards to study how the evolution of development shapes the capacity for continued evolution, or evolvability.

Theo, Yang, Mara and Valentina hard at work this Arpil

A second long-term goal is to understand what, if anything, will make the introgression stop? Our phenotypic sampling has revealed a potential kryptonite to the Tuscan phenotype – high altitude. The introgressive spread of the Tuscan phenotype is restricted in the mountains and in some cases cease altogether, resulting in the persistence of the brown backed morph at the highest altitudes. There are several potential explanations for this, including geographic barriers or selection. This year we added two new detectives to the team, Mara and Theo, whose projects are designed to address this question.

Mara enjoying her first field season…

So the wall lizard story continues. As one chapter draws to a close new research questions have emerged allowing us to continue our spring forays to the land of pizza, pasta and lucertole. Now with the genome at our hands, the opportunities to explore these questions at both a phenotypic and genomic level have never been greater. Let us know if you’d like to join us.

For the published work to date, please see the following papers

MacGregor, H.E.A., While, G.M. and Uller, T. (2017) Comparison of reproductive investment in native and non-native populations of common wall lizards reveals sex differences in adaptive potential. Oikos. In press.

While, G.M. and Uller, T. (2017) Female reproductive investment in response to male phenotype in wall lizards and its implications for introgression. Biological Journal of the Linnean Society. In press.

MacGregor, H.E.A., While, G. M., Barret, J., Perez l de Lanuza, G., Carazo, P., Michaelides, S. and Uller T. (2017) Experimental contact zones reveal the causes and targets of sexual selection in hybrid zones. Functional Ecology, 31:742-752.

Heathcote, R.J.P., While, G.M., MacGregor, H.E.A., Sciberras, J., Leroy, C., d’Ettorre, P. and Uller, T. (2016) Male behaviour drives assortative reproduction during the initial stages of secondary contact. Journal of Evolutionary Biology, 29:1003-1015.

While, G, M., Michaelides, S., Heathcote, R.J.P., MacGregor, H.E.A., Zajac, N., Beninde, J., Carazo, P., Perez I de Lanuza, G., Sacchi, R., Zuffi, M., Horvathova, T., Fresnillo, B., Schulte, U., Veith, M., Hochkirch, A. and Uller, T. (2015) Sexual selection drives asymmetric introgression in wall lizards. Ecology Letters, 18:1366-1375.