Final Report: Predicting
and monitoring climate change in insects:
from genes to distribution shifts
Investigators:
Ary Hoffmann (University of Melbourne) (chief investigator)
Carla Sgro (Monash University)
Scott Ritchie (James Cook University)
Craig Williams (University of South Australia)
Michael Kearney (University of Melbourne)
Peter Ryan (Queensland Institute of Medical Research)
Report date: December 2010
Summary of application: We need methods to effectively predict the risk of invasions of health/agricultural
pest organisms, and the risk of extinction of threatened organisms, if we are to mitigate future changes in
climate. We will use insects from threatened habitats and Aedes mosquitoes (vectors of dengue fever) to
implement a new approach for predicting the future distribution of key species with climate change. Our
approach links genetic markers and GIS data with powerful new mechanistic models that allows us to predict
the impact of both evolutionary potential and changed human behaviour on the future distribution of species.
Commonwealth Environment Research Facilities – Significant Project
Summary of the major activities undertaken by the organisation
We tested more than 50 genetic markers for their involvement in climatic adaptation in a variety of
ways. Using RNAi techniques, several markers were identified that affected cold and desiccation
resistance, including heat shock genes, starvin, ebony and frost. We have shown that there has been
a selective sweep around markers in the rainforest restricted species of Drosophila and we have
identified several polymorphisms and non-functional genes. Several of the polymorphisms were linked
to trait variation. We also used selection experiments and DNA hybridization to associate several
genes with variation in desiccation resistance. Finally, the heritability of stress resistance was
investigated in multiple Drosophila species to test the notion that genetic variation and stress
sensitivity are linked. This component of the project contributed to 8 papers and two workshops,
involved two postdoctoral researchers and also supported 3 students.
We developed trait-based mechanistic models that use energy balance equations to predict how
climate will directly affect organisms under different climate scenarios. Physiological data were
collected to fit parameters to the models and a novel evolutionary component was developed to
investigate how evolved changes in a key trait (egg desiccation) would influence predicted
distributions under climate change. We also collected data on the thermal properties of various types
of water storage receptacles and modeled their suitability as breeding sites. Population comparisons
were completed to investigate local adaptation and genetic variation in the mosquitoes. This extended
to investigations of how different populations performed in terms of fecundity, mating success, and
locomotion in various temperature regimes. Such work has helped us to understand the extent of
local adaptation.
An existing mechanistic model was used to investigate the extinction processes currently working
against Aedes aegypti populations in Australia. This work provided a cross-validation for the traitbased mechanistic models (mentioned above), highlighted the important environmental factors
limiting current distribution of this species, and enabled a risk assessment of future distribution
expansion. This work provided further evidence that egg longevity (mediated by desiccation
resistance) is a key trait limiting the distribution of this species.
We also undertook household surveys for dengue mosquito immatures (larvae/pupae) and
contemporary water storage container habitats in representative areas of Brisbane. These surveys
provided important contextual information on recent changes in human behaviour, largely in response
to changing weather patterns that may indirectly affect the abundance and distribution of Aedes
aegypti in Queensland. The explosion in the abundance of peridomestic water storage containers in
houses in south east Queensland (currently in 65% of houses), compared with their almost complete
absence from houses fifteen years ago, represents an important change in the potential receptivity of
south east Queensland (pop 2.8 million) to the re-introduction of dengue vectors.
An outline of any demonstration/communication activities undertaken (as specified in Item 1 of the
Schedule)
Three workshops were run as part of the project. A workshop entitled “dengue and mosquito vectors
in southern Queensland and other areas: what is the likely threat and what can we do about it?” was
run in Brisbane in 2010 and attracted a variety of council workers, Queensland Health officials, and
environmental managers. A workshop entitled “genetic translocations and adaptation under climate
change; theory and practise” was run in Melbourne in 2010. The workshop attracted participants from
the Department of Sustainability and Environment (Victoria), Department of Conservation and Land
Management (Western Australia), CSIRO, and several universities and NGOs. A workshop entitled
“genetic approaches to climate change adaptation” was run in Canberra in 2009. This workshop was
well attended by Commonwealth Government DEWHA representatives.
A total of 11 publications have so far been produced during the project (more papers pending). A
highlight of the project was the first demonstration of a link between trait heritability, species
distributions and physiological limits published in Science which provides a new understanding of the
genetic basis of evolutionary limits and the identification of species lineages that are particularly
susceptible to climate change. They also include a major review published in Nature Reviews
Genetics on genetic markers for climate adaptation, and several papers on candidate genes identified
through association studies and gene knockout assays. The project also produced an important paper
published in Functional Ecology where mechanistic models were first used to predict the likely effects
of climate change on the dengue vector Aedes aegypti in northern Australia and for the first time
incorporated evolutionary components into species distribution prediction. Two follow up papers
highlight the importance of local knowledge in predicting species responses and the dangers posed
by tyres in propagating mosquito populations under extreme conditions. The candidate gene list and
distribution changes have both been presented on line and the mosquito distribution work generated
substantial interest from the print and television media.
The results of the household surveys in representative areas of Brisbane have been communicated
broadly to local and state governments, particularly Brisbane City Council which is the largest Local
Government in Australia (Population 1,052,458). Based on the results from the CERF Project,
Brisbane City Council have agreed to undertake broad surveys across all of Brisbane's 158 Statistical
Local Areas (total of 10,000 households to be surveyed). This work will identify high risk areas for the
establishment of dengue mosquitoes, which can then form the basis of a prioritised approach to
monitoring of climate related range expansions in medically important insect species.
The benefits and outcomes of the Activity as a whole
The project has provided a new and sophisticated approach to understanding the likely effects of
climate change in the distribution of pest species. This is the first time that mechanistic models have
been applied to a pest species and the resulting models demonstrate the potential for dengue vectors
to spread to Darwin and to southern locations as long as breeding containers are available. The
project has also developed new methods for species distribution modelling incorporating evolution
that should be equally applicable to other pest species and species of conservation concern. The
project has highlighted the thermal buffering capacity of tyres as containers with the potential to
support mosquito populations even in unfavourable areas, and it has demonstrated for the first time
the presence of local adaptation in mosquito populations suggesting adaptive shifts.
The project provides a major breakthrough in how adaptive limits are regarded in species. This is the
first demonstration that genetic limits underlie ecological limits in species, forcing lineages to be
restricted to moist environments from which they cannot easily expand. The results raise the issue
that vulnerability of species can be identified from species genomes, an idea that remains to be tested
through genomic comparisons in the future. These results have been presented to numerous forums
and stimulated discussion around physiological limits and the genomic basis of biodiversity. The
adaptive markers identified in the project have been widely reported in the literature and should help
to stimulate the use of adaptive markers for routine monitoring of populations. The markers are
already being used in the identification of pollution effects.
The project has identified several issues of concern for health authorities in dealing with mosquitoes.
Water storage containers are a risk to produce Ae. aegypti mosquitoes, and regulatory efforts should
be made to ensure they are "mosquito proof". Furthermore, local government should consider public
education and inspections of domestic rain water storage systems to prevention the potential reemergence of Ae. aegypti in some urban areas, particularly the large population centres in south east
Queensland (total population 3 million) where Ae. aegypti are currently absent.
The degree to which the Activity has effectively achieved its objectives (each objective should be
discussed separately)
The project successfully achieved all its objectives. We pointed out that to manage species responses
to climate change, it is crucial that we identify species most at risk from climate change before they
become threatened by extinction, and then implement appropriate management strategies. We
carried out extensive heritability experiments to test the notion that evolutionary potential can be
limited in species. We also developed a series of genetic markers for monitoring the early impacts of
climate change on species distributions and abundances.
We aimed to link the traits of the organism (rather than its distribution) to GIS data to predict their
distribution. We showed how mechanistic models can be developed to predict the likely spread of the
dengue fever transmission vector, Aedes aegypti, under climate change. The project identified key
mosquito traits that determine its distribution and evaluated the potential for evolution to change these
traits and further expand the Ae. aegypti distribution. The research program led to the discovery of
genes indicative of adaptive potential well beyond the experimental system proposed.The approach
developed in this proposal serves as a template for predicting changes in disease vectors and
agricultural pests. It also serves as a template for rapid genetic approaches in screening threatened
species.
The surveys in south east Queensland highlighted the important role that human adaptation strategies
may play in future distribution of medically important insects. In south east Queensland, local
government mosquito control programs do not routinely target mosquitoes in and around houses.
However, these mosquitoes, commonly referred to as ‘container breeders’, can impact on human
health and lifestyle. Previously, natural habitats, mainly bromeliad axils, garden accoutrements and
discarded items were the most productive habitats for container mosquitoes in south east
Queensland. This project has identified contemporary household water storage patterns in Brisbane
over two consecutive Winter and Summer periods (2008-2009), including an explosion in the numbers
of water storage containers. Now, almost one in two houses have a rainwater tank and in some
suburbs up to a third of householders are collecting water in buckets, drums and other containers.
This phenomenon is a direct result of water shortages and public policies to encourage house water
conservation and storage. Intentionally filling (garden accoutrements) or harvesting (water storage
containers) of water provides suitable, year round, habitat for container breeding mosquitoes,
potentially increasing the receptivity of urban Brisbane to dengue vectors. This empirical information,
combined with the mechanistic models that have been developed as part of this project, will provide a
sound basis for the development of public health policy to manage these threats.
The appropriateness of the approaches used in the development and implementation of the Activity
The approaches we used in the project were adequate to tackle the main aims of the project. The
heritability studies across species were completed successfully and were adequate to test the
hypothesis that genetic variance can limit adaptive responses. The DNA hybridization and marker
association approaches we adopted to identify candidates worked well and many new candidates
were subsequently tested for functional significance in RNAi assays. We also successfully extended
the markers to other species although progress in this area was perhaps slower than we might have
hoped for mainly associated with PCR problems.
The mechanistic model for predicting the historical distribution and future spread of Aedes aegypti
was successfully developed and implemented, and the use of existing models enabled an
investigation of extinction processes in this species. We identified key life history traits limiting
distributions and tested for genetic variation in these traits as well as adaptive divergence. We
showed that there was some evidence of divergence among populations in the expected direction.
Our microclimatic measurements of containers were successful in highlighting containers of concern
for mosquito surveillance particularly as climate variability increases. The survey results were
successful in demonstrating the potential risks posed by rainwater tanks as a reservoir for mosquito
populations although additional surveys are required to establish risks across Brisbane. Based on the
results from the CERF Project, Brisbane City Council have agreed to undertake broad surveys across
all of Brisbane's 158 Statistical Local Areas (total of 10,000 households to be surveyed).
Papers
Hoffmann, A. A. Willi, Y. (2008) Detecting genetic responses to environmental change. Nature
Reviews Genetics 9:421-432
Kellermann, V. van Heerwaarden, B. Sgrò, C.M. Hoffmann, A.A. (2009). Fundamental evolutionary
limits in ecological traits drive Drosophila species distributions. Science 325: 1244-1246.
Kearney, M., Porter, W.P., Williams, C., Ritchie, S., Hoffmann, A.A, (2009) Integrating biophysical
models and evolutionary theory to predict climatic impacts on species’ ranges: the dengue mosquito
Aedes aegypti in Australia. Functional Ecology 23: 528-538.
McKechnie, S.W. Blacket, M. Song, S. Rako, L. Caroll, X. Johnson, T.K. Jensen, L.T. Lee, S.F. Wee, C.W.
Hoffmann, A.A. (2010). A clinally-varying promoter polymorphism associated with adaptive variation
in wing size in Drosophila. Molecular Ecology 19: 775-784
Colinet, H. Lee, S.F., Hoffmann, A.A. (2010). Temporal expression of heat shock genes during cold
stress and recovery from chill coma in adult Drosophila melanogaster. FEBS Journal doi:10.1111/j.17424658.2009.07470.x.
Mitchell, K.A. Hoffmann, A.A. (2010). Thermal ramping rate influences evolutionary potential and
species differences for upper thermal limits in Drosophila. Functional Ecology 24: 694-700
Colinet, H. Hoffmann, A.A. (2010) Gene and protein expression of Drosophila Starvin during cold
stress and recovery from chill coma Insect Biochemistry and Molecular Biology Biology 40: 425-8
Colinet, H. Lee, S.F. Hoffmann, A. A. (2010). Knocking down expression of Hsp22 and Hsp23 by RNA
interference affects recovery from chill coma in Drosophila melanogaster. Journal of Experimental
Biology 213:4146-4150.
Colinet, H. Lee, S. F. Hoffmann, A.A. (2010). Functional characterization of the Frost gene in
Drosophila melanogaster: importance for recovery from chill coma. PLOS One 5: e10925.
Hoffmann, A.A. (2010) A genetic perspective on insect climate specialists. Australian Journal of
Entomology 49: 93-101.
Mitchell, K.A. Sgrò, C.M. Hoffmann, A.A. (2011). Phenotypic plasticity in upper thermal limits is
weakly related to Drosophila species distributions. Functional Ecology (early view)