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.