Category Archives: Published paper

Cross-study comparison reveals common genomic, network, and functional signatures of desiccation resistance in Drosophila melanogaster

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Authors: Marina Telonis-Scott, Carla M Sgrò, Ary A Hoffmann and Philippa C Griffin

Published in: Molecular Biology and Evolution (early view)

Abstract

Repeated attempts to map the genomic basis of complex traits often yield different outcomes because of the influence of genetic background, gene-by-environment interactions, and/or statistical limitations. However, where repeatability is low at the level of individual genes, overlap often occurs in gene ontology categories, genetic pathways, and interaction networks.

Here we report on the genomic overlap for natural desiccation resistance from a Pool-genome-wide association study experiment and a selection experiment in flies collected from the same region in southeastern Australia in different years.

We identified over 600 single nucleotide polymorphisms associated with desiccation resistance in flies derived from almost 1,000 wild-caught genotypes, a similar number of loci to that observed in our previous genomic study of selected lines, demonstrating the genetic complexity of this ecologically important trait.

By harnessing the power of cross-study comparison, we narrowed the candidates from almost 400 genes in each study to a core set of 45 genes, enriched for stimulus, stress, and defense responses.

In addition to gene-level overlap, there was higher order congruence at the network and functional levels, suggesting genetic redundancy in key stress sensing, stress response, immunity, signaling, and gene expression pathways. We also identified variants linked to different molecular aspects of desiccation physiology previously verified from functional experiments.

Our approach provides insight into the genomic basis of a complex and ecologically important trait and predicts candidate genetic pathways to explore in multiple genetic backgrounds and related species within a functional framework.

Citation

Telonis-Scott M, Sgrò CM, Hoffmann AA, Griffin PC (2016) Cross-study comparison reveals common genomic, network and functional signatures of desiccation resistance in Drosophila melanogaster. Molecular Biology and Evolution PDF DOI

What can plasticity contribute to insect responses to climate change?

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Authors: Carla M Sgro, John S Terblanche and Ary A Hoffmann

Published in: Annual Reviews of Entomology, volume 61 (March 2016)

Abstract

Plastic responses figure prominently in discussions on insect adaptation to climate change.

Here we review the different types of plastic responses and whether they contribute much to adaptation.

Under climate change, plastic responses involving diapause are often critical for population persistence, but key diapause responses under dry and hot conditions remain poorly understood.

Climate variability can impose large fitness costs on insects showing diapause and other life cycle responses, threatening population persistence.

In response to stressful climatic conditions, insects also undergo ontogenetic changes including hardening and acclimation. Environmental conditions experienced across developmental stages or by prior generations can influence hardening and acclimation, although evidence for the latter remains weak. Costs and constraints influence patterns of plasticity across insect clades, but they are poorly understood within field contexts.

Plastic responses and their evolution should be considered when predicting vulnerability to climate change—but meaningful empirical data lag behind theory.

Citation

Sgrò CM, Terblanche J, Hoffmann AA (2016) What can plasticity contribute to insect respones to climate change? Annual Reviews of Entomology PDF DOI

Increases in the evolutionary potential of upper thermal limits under warmer temperatures in two rainforest Drosophila species

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Authors: Belinda van Heerwaarden, Michelle Malmberg and Carla M Sgrò

Published in: Evolution (early view)

Abstract

Tropical and subtropical species represent the majority of biodiversity. These species are predicted to lack the capacity to evolve higher thermal limits in response to selection imposed by climatic change. However, these assessments have relied on indirect estimates of adaptive capacity, using conditions that do not reflect environmental changes projected under climate change.

Using a paternal half-sib full-sib breeding design, we estimated the additive genetic variance and narrow-sense heritability for adult upper thermal limits in two rainforest-restricted species of Drosophila reared under two thermal regimes, reflecting increases in seasonal temperature projected for the wet tropics of Australia and under standard laboratory conditions (constant 25‌°C).

Estimates of additive genetic variation and narrow-sense heritability for adult heat tolerance were significantly different from zero in both species under projected summer, but not winter or constant, thermal regimes. In contrast, significant broad-sense genetic variation was apparent in all thermal regimes for egg-to-adult viability.

Environment-dependent changes in the expression of genetic variation for adult upper thermal limits suggest that predicting adaptive responses to climate change will be difficult.

Estimating adaptive capacity under conditions that do not reflect future environmental conditions may provide limited insight into evolutionary responses to climate change.

Citation

van Heerwaarden B, Malmburg M, Sgrò CM (2016) Increases in the evolutionary potential of upper thermal limits under warmer temperatures in two rainforest Drosophila species. Evolution PDF DOI

Revealing hidden evolutionary capacity to cope with global change

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Authors: Evatt Chirgwin, Keyne Monro, Carla M Sgrò and Dustin J Marshall

Published in: Global Change Biology, volume 21, issue 9 (September 2015)

Abstract

The extent to which global change will impact the long-term persistence of species depends on their evolutionary potential to adapt to future conditions.

While the number of studies that estimate the standing levels of adaptive genetic variation in populations under predicted global change scenarios is growing all the time, few studies have considered multiple environments simultaneously and even fewer have considered evolutionary potential in multi- variate context.

Because conditions will not be constant, adaptation to climate change is fundamentally a multivariate process so viewing genetic variances and covariances over multivariate space will always be more informative than relying on bivariate genetic correlations between traits. A multivariate approach to understanding the evolutionary capacity to cope with global change is necessary to avoid misestimating adaptive genetic variation in the dimensions in which selection will act.

We assessed the evolutionary capacity of the larval stage of the marine polychaete Galeolaria caespitosa to adapt to warmer water temperatures. Galeolaria is an important habitat-forming species in Australia, and its earlier life-history stages tend to be more susceptible to stress. We used a powerful quantitative genetics design that assessed the impacts of three temperatures on subsequent survival across over 30,000 embryos across 204 unique families.

We found adaptive genetic variation in the two cooler temperatures in our study, but none in the warmest temperature. Based on these results, we would have concluded that this species has very little capacity to evolve to the warmest temperature. However, when we explored genetic variation in multivariate space, we found evidence that larval survival has the potential to evolve even in the warmest temperatures via correlated responses to selection across thermal environments.

Future studies should take a multivariate approach to estimating evolutionary capacity to cope with global change lest they misestimate a species’ true adaptive potential.

Citation

Chirgwin E, Monro K, Sgrò CM, Marshall DJ (2015) Revealing hidden evolutionary capacity to cope with global change. Global Change Biology PDF DOI

Low evolutionary potential for egg-to-adult viability in Drosophila melanogaster at high temperatures

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Authors: Torsten N Kristensen, Johannes Overgaard, Jan Lassen, Ary A Hoffmann, and Carla Sgrò

Published in: Evolution, volume 69, issue 3 (March 2015)

Abstract

To cope with the increasing and less-predictable temperature forecasts under climate change, many terrestrial ectotherms will have to migrate or rely on adaptation through plastic or evolutionary means.

Studies suggest that some ectotherms have a limited potential to change their upper thermal limits via evolutionary shifts, but research has mostly focused on adult life stages under laboratory conditions.

Here we use replicate populations of Drosophila melanogaster and a nested half-sib/full-sib quantitative genetic design to estimate heritabilities and genetic variance components for egg-to-adult viability under both laboratory and seminatural field conditions, encompassing cold, benign, and hot temperatures in two separate populations.

The results demonstrated temperature-specific heritabilities and additive genetic variances for egg-to-adult viability. Heritabilities and genetic variances were higher under cold and benign compared to hot temperatures when tested under controlled laboratory conditions. Tendencies toward lower evolutionary potential at higher temperatures were also observed under seminatural conditions although the results were less clear in the field setting.

Overall the results suggest that ectotherms that already experience temperatures close to their upper thermal tolerance limits have a restricted capacity to adapt to higher temperatures by evolutionary means.

Citation

Kristensen TN, Overgaard J, Lassen J, Hoffmann, AA and Sgrò CM (2015). Low evolutionary potential for egg‐to‐adult viability in Drosophila melanogaster at high temperatures. Evolution PDF DOI

A framework for incorporating evolutionary genomics into biodiversity conservation and management

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Authors: Ary Hoffmann, Philippa Griffin, Shannon Dillon, Renee Catullo, Rahul Rane, Margaret Byrne, Rebecca Jordan, John Oakeshott, Andrew Weeks, Leo Joseph, Peter Lockhart, Justin Borevitz and Carla Sgrò

Published in: Climate Change Responses, volume 2, issue 1 (January 2015)

Abstract

Evolutionary adaptation drives biodiversity. So far, however, evolutionary thinking has had limited impact on plans to counter the effects of climate change on biodiversity and associated ecosystem services. This is despite habitat fragmentation diminishing the ability of populations to mount evolutionary responses, via reductions in population size, reductions in gene flow and reductions in the heterogeneity of environments that populations occupy.

Research on evolutionary adaptation to other challenges has benefitted enormously in recent years from genomic tools, but these have so far only been applied to the climate change issue in a piecemeal manner.

Here, we explore how new genomic knowledge might be combined with evolutionary thinking in a decision framework aimed at reducing the long-term impacts of climate change on biodiversity and ecosystem services. This framework highlights the need to rethink local conservation and management efforts in biodiversity conservation.

We take a dynamic view of biodiversity based on the recognition of continuously evolving lineages, and we highlight when and where new genomic approaches are justified.

In general, and despite challenges in developing genomic tools for non-model organisms, genomics can help management decide when resources should be redirected to increasing gene flow and hybridisation across climate zones and facilitating in situ evolutionary change in large heterogeneous areas. It can also help inform when conservation priorities need to shift from maintaining genetically distinct populations and species to supporting processes of evolutionary change.

We illustrate our argument with particular reference to Australia’s biodiversity.

Citation

Hoffmann AA, Griffin P, Dillon S, Catullo R, Rane R, Byrne M, Jordan R, Oakeshott J, Weeks AR, Joseph L, Lockhart P, Borevitz J, Sgrò CM (2015) A framework for incorporating evolutionary genomics into biodiversity conservation and management. Climate Change Responses PDF DOI

Spatial analysis of gene regulation reveals new insights into the molecular basis of upper thermal limits

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Authors: Marina Telonis-Scott, Allannah S Clemson, Travis K Johnson and Carla M Sgrò

Published in: Molecular Ecology, volume 23, issue 24 (December 2014)

Abstract

The cellular stress response has long been the primary model for studying the molecular basis of thermal adaptation, yet the link between gene expression, RNA metabolism and physiological responses to thermal stress remains largely unexplored.

We address this by comparing the transcriptional and physiological responses of three geographically distinct populations of Drosophila melanogaster from eastern Australia in response to, and recovery from, a severe heat stress with and without a prestress hardening treatment.

We focus on starvin (stv), recently identified as an important thermally responsive gene. Intriguingly, stv encodes seven transcripts from alternative transcription sites and alternative splicing, yet appears to be rapidly heat inducible.

First, we show genetic differences in upper thermal limits of the populations tested. We then demonstrate that the stv locus does not ubiquitously respond to thermal stress but is expressed as three distinct thermal and temporal RNA phenotypes (isoforms). The shorter transcript isoforms are rapidly upregulated under stress in all populations and show similar molecular signatures to heat-shock proteins. Multiple stress exposures seem to generate a reserve of pre-mRNAs, effectively ‘priming’ the cells for subsequent stress.

Remarkably, we demonstrate a bypass in the splicing blockade in these isoforms, suggesting an essential role for these transcripts under heat stress. Temporal profiles for the weakly heat responsive stv isoform subset show opposing patterns in the two most divergent populations. Innate and induced transcriptome responses to hyperthermia are complex, and warrant moving beyond gene-level analyses.

Citation

Telonis-Scott, M, Clemson AS, Johnson TK, Sgrò, CM (2014) Spatial analysis of gene regulation reveals new insights into the molecular basis of upper thermal limits,
Molecular Ecology PDF DOI

No patterns in thermal plasticity along a latitudinal gradient in Drosophila simulates from eastern Australia

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Authors: Belinda van Heerwaarden, Richard Foo Heng Lee, Johannes Overgaard and Carla M Sgrò

Published in: Journal of Evolutionary Biology, volume 27, issue 11 (November 2014)

Abstract

Phenotypic plasticity may be an important initial mechanism to counter environmental change, yet we know relatively little about the evolution of plasticity in nature.

Species with widespread distributions are expected to have evolved higher levels of plasticity compared with those with more restricted, tropical distributions.

At the intraspecific level, temperate populations are expected to have evolved higher levels of plasticity than their tropical counterparts. However, empirical support for these expectations is limited. In addition, no studies have comprehensively examined the evolution of thermal plasticity across life stages.

Using populations of Drosophila simulans collected from a latitudinal cline spanning the entire east coast of Australia, we assessed thermal plasticity, measured as hardening capacity (the difference between basal and hardened thermal tolerance) for multiple measures of heat and cold tolerance across both adult and larval stages of development. This allowed us to explicitly ask whether the evolution of thermal plasticity is favoured in more variable, temperate environments.

We found no relationship between thermal plasticity and latitude, providing little support for the hypothesis that temperate populations have evolved higher levels of thermal plasticity than their tropical counterparts.

With the exception of adult heat survival, we also found no association between plas- ticity and ten climatic variables, indicating that the evolution of thermal plasticity is not easily predicted by the type of environment that a particular population occupies. We discuss these results in the context of the role of plasticity in a warming climate.

Citation

van Heerwaarden B, Lee RFH, Overgaard J, Sgrò CM (2014) No patterns in thermal plasticity along a latitudinal gradient in Drosophila simulans from eastern Australia. Journal of Evolutionary Biology PDF DOI

Is adaptation to climate change really constrained in niche specialists?

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Authors: Belinda van Heerwaarden and Carla M Sgrò

Published in: Proceedings of the Royal Society B, volume 281, number 1790 (September 2014)

Abstract

Species with restricted distributions make up the vast majority of biodiversity.

Recent evidence suggests that Drosophila species with restricted tropical distributions lack genetic variation in the key trait of desiccation resistance. It has therefore been predicted that tropically restricted species will be limited in their evolutionary response to future climatic changes and will face higher risks of extinction. However, these assessments have been made using extreme levels of desiccation stress (less than 10% relative humidity (RH)) that extend well beyond the changes projected for the wet tropics under climate change scenarios over the next 30 years.

Here, we show that significant evolutionary responses to less extreme (35% RH) but more ecologically realistic levels of climatic change and desiccation stress are in fact possible in two species of rainforest restricted Drosophila. Evolution may indeed be an important means by which sensitive rainforest-restricted species are able to mitigate the effects of climate change.

Citation

van Heerwaarden, B Sgrò CM (2014) Is adaptation to climate change really constrained in niche specialists? Proceedings of the Royal Society B PDF DOI

Evolutionary capacity of upper thermal limits: beyond single trait assessments

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Authors: Shaun Blackburn, Belinda van Heerwaarden, Vanessa Kellermann and Carla M Sgrò

Published in: Journal of Experimental Biology, volume 217, number 11 (June 2014)

Abstract

Thermal tolerance is an important factor influencing the distribution of ectotherms, but we still have limited understanding of the ability of species to evolve different thermal limits.

Recent studies suggest that species may have limited capacity to evolve higher thermal limits in response to slower, more ecologically relevant rates of warming. However, these conclusions are based on univariate estimates of adaptive capacity.

To test these findings within an explicitly multivariate context, we used a paternal half-sibling breeding design to estimate the multivariate evolutionary potential for upper thermal limits in Drosophila melanogaster. We assessed heat tolerance using static (basal and hardened) and ramping assays.

Additive genetic variances were significantly different from zero only for the static measures of heat tolerance. Our G matrix analysis revealed that any response to selection for increased heat tolerance will largely be driven by static basal and hardened heat tolerance, with minimal contribution from ramping heat tolerance.

These results suggest that the capacity to evolve upper thermal limits in nature may depend on the type of thermal stress experienced.

Citation

Blackburn S, van Heerwaarden B, Kellermann V, Sgrò CM (2014) Evolutionary capacity of upper thermal limits: beyond single trait assessments. Journal of Experimental Biology PDF DOI