How important is thermal history? Evidence for lasting effects of developmental temperature on upper thermal limits in Drosophila melanogaster

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

Published in: Proceedings of the Royal Society B, volume 284, issue 1855 (May 2017)

Abstract

A common practice in thermal biology is to take individuals directly from the field and estimate a range of thermal traits. These estimates are then used in studies aiming to understand broad scale distributional patterns, understanding and predicting the evolution of phenotypic plasticity, and generating predictions for climate change risk. However, the use of field-caught individuals in such studies ignores the fact that many traits are phenotypically plastic and will be influenced by the thermal history of the focal individuals.

The current study aims to determine the extent to which estimates of upper thermal limits (CTmax), a frequently used measure for climate change risk, are sensitive to developmental and adult acclimation temperatures and whether these two forms of plasticity are reversible.

Examining a temperate and tropical population of Drosophila melanogaster we show that developmental acclimation has a larger and more lasting effect on CTmax than adult acclimation. We also find evidence for an interaction between developmental and adult acclimation, particularly when flies are acclimated for a longer period, and that these effects can be population specific.

These results suggest that thermal history can have lasting effects on estimates of CTmax. In addition, we provide evidence that developmental and/or adult acclimation are unlikely to contribute to substantial shifts in CTmax and that acclimation capacity may be constrained at higher temperatures.

Citation

Kellermann V, van Heerwaarden B, Sgrò CM (2017) How important is thermal history? Evidence for lasting effects of developmental temperature on upper thermal limits in Drosophila melanogaster. Proceedings of the Royal Society of London B, PDF DOI

Revisiting adaptive potential, population size, and conservation

Authors: Ary A Hoffmann, Carla M Sgrò, and Torsten N Kristensen

Published in: Trends in Ecology and Evolution, volume 32, issue 7 (July 2017)

Abstract

Additive genetic variance (VA) reflects the potential for evolutionary shifts and can be low for some traits or populations.

High VA is critical for the conservation of threatened species under selection to facilitate adaptation.

Theory predicts tight associations between population size and VA, but data from some experimental models, and managed and natural populations do not always support this prediction. However, VA comparisons often have low statistical power, are undertaken in highly controlled environments distinct from natural habitats, and focus on traits with limited ecological relevance. Moreover, investigations of VA typically fail to consider rare alleles, genetic load, or linkage disequilibrium, resulting in deleterious effects associated with favored alleles in small populations.

Large population size remains essential for ensuring adaptation.

Citation

Hoffmann AA, Sgrò CM, Kristensen TN (2017) Revisiting adaptive potential, population size, and conservation, Trends in Ecology and Evolution, PDF DOI

Aligning science and policy to achieve evolutionarily enlightened conservation

Authors: Carly N Cook and Carla M Sgrò

Published in: Conservation Biology (early view)

Abstract

There is increasing recognition among conservation scientists that long-term conservation outcomes could be improved through better integration of evolutionary theory into management practices. Despite concerns that the importance of key concepts emerging from evolutionary theory (i.e., evolutionary principles and processes) are not being recognized by managers, there has been little effort to determine the level of integration of evolutionary theory into conservation policy and practice.

We assessed conservation policy at 3 scales (international, national, and provincial) on 3 continents to quantify the degree to which key evolutionary concepts, such as genetic diversity and gene flow, are being incorporated into conservation practice. We also evaluated the availability of clear guidance within the applied evolutionary biology literature as to how managers can change their management practices to achieve better conservation outcomes.

Despite widespread recognition of the importance of maintaining genetic diversity, conservation policies provide little guidance about how this can be achieved in practice and other relevant evolutionary concepts, such as inbreeding depression, are mentioned rarely. In some cases the poor integration of evolutionary concepts into management reflects a lack of decision-support tools in the literature. Where these tools are available, such as risk-assessment frameworks, they are not being adopted by conservation policy makers, suggesting that the availability of a strong evidence base is not the only barrier to evolutionarily enlightened management.

We believe there is a clear need for more engagement by evolutionary biologists with policy makers to develop practical guidelines that will help managers make changes to conservation practice. There is also an urgent need for more research to better understand the barriers to and opportunities for incorporating evolutionary theory into conservation practice.

Citation

Cook CN, Sgrò CM (2017) Aligning science and policy to achieve evolutionarily enlightened conservation. Conservation Biology, PDF DOI

Sex-biased transcriptome divergence along a latitudinal gradient

Authors: Scott L Allen, Russell Bonduriansky, Carla M Sgrò, and Stephen F. Chenoweth

Published in: Molecular Ecology, volume 26, issue 5 (March 2017)

Abstract

Sex-dependent gene expression is likely an important genomic mechanism that allows sex-specific adaptation to environmental changes.

Among Drosophila species, sex-biased genes display remarkably consistent evolutionary patterns; male-biased genes evolve faster than unbiased genes in both coding sequence and expression level, suggesting sex differences in selection through time. However, comparatively little is known of the evolutionary process shaping sex-biased expression within species. Latitudinal clines offer an opportunity to examine how changes in key ecological parameters also influence sex-specific selection and the evolution of sex-biased gene expression.

We assayed male and female gene expression in Drosophila serrata along a latitudinal gradient in eastern Australia spanning most of its endemic distribution. Analysis of 11,631 genes across eight populations revealed strong sex differences in the frequency, mode and strength of divergence. Divergence was far stronger in males than females and while latitudinal clines were evident in both sexes, male divergence was often population specific, suggesting responses to localized selection pressures that do not covary predictably with latitude.

While divergence was enriched for male-biased genes, there was no overrepresentation of X-linked genes in males. By contrast, X-linked divergence was elevated in females, especially for female-biased genes. Many genes that diverged in D. serrata have homologs also showing latitudinal divergence in Drosophila simulans and Drosophila melanogaster on other continents, likely indicating parallel adaptation in these distantly related species.

Our results suggest that sex differences in selection play an important role in shaping the evolution of gene expression over macro- and micro-ecological spatial scales.

Citation

Allen SL, Bonduriansky R, Sgro CM and Chenoweth SF (2017) Sex-biased transcriptome divergence along a latitudinal gradient. Molecular Ecology, PDF DOI

The relative contributions of the X chromosome and autosomes to local adaptation

Authors: Clémentine Lasne, Carla M Sgrò, and Tim Connallon

Published in: Genetics, volume 205, issue 4 (April 2017)

Abstract

Models of sex chromosome and autosome evolution yield key predictions about the genomic basis of adaptive divergence, and such models have been important in guiding empirical research in comparative genomics and studies of speciation.

In addition to the adaptive differentiation that occurs between species over time, selection also favors genetic divergence across geographic space, with subpopulations of single species evolving conspicuous differences in traits involved in adaptation to local environmental conditions. The potential contribution of sex chromosomes (the X or Z) to local adaptation remains unclear, as we currently lack theory that directly links spatial variation in selection to local adaptation of X-linked and autosomal genes.

Here, we develop population genetic models that explicitly consider the effects of genetic dominance, effective population size, and sex-specific migration and selection, on the relative contributions of X-linked and autosomal genes to local adaptation.

We show that X-linked genes should nearly always disproportionately contribute to local adaptation in the presence of gene flow. We also show that considerations of dominance and effective population size — which play pivotal roles in the theory of faster-X adaptation between species — have surprisingly little influence on the relative contribution of the X chromosome to local adaptation. Instead, sex-biased migration is the primary mediator of the strength of spatial large-X effects.

Our results yield novel predictions about the role of sex chromosomes in local adaptation. We outline empirical approaches in evolutionary quantitative genetics and genomics that could build upon this new theory.

Citation

Lasne C, Sgrò CM, Connallon T (2017) The relative contributions of the X chromosome and autosomes to local adaptation. Genetics, PDF DOI

The other 96%: Can neglected sources of fitness variation offer new insights into adaptation to global change?

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

Published in: Evolutionary Applications, volume 10, issue 3 (March 2017)

Abstract

Mounting research considers whether populations may adapt to global change based on additive genetic variance in fitness. Yet selection acts on phenotypes, not additive genetic variance alone, meaning that persistence and evolutionary potential in the near term, at least, may be influenced by other sources of fitness variation, including nonadditive genetic and maternal environmental effects. The fitness consequences of these effects, and their environmental sensitivity, are largely unknown.

Here, applying a quantitative genetic breeding design to an ecologically important marine tubeworm, we examined nonadditive genetic and maternal environmental effects on fitness (larval survival) across three thermal environments.

We found that these effects are nontrivial and environment dependent, explaining at least 44% of all parentally derived effects on survival at any temperature and 96% of parental effects at the most stressful temperature. Unlike maternal environmental effects, which manifested at the latter temperature only, nonadditive genetic effects were consistently significant and covaried positively across temperatures (i.e., parental combinations that enhanced survival at one temperature also enhanced survival at elevated temperatures).

Thus, while nonadditive genetic and maternal environmental effects have long been neglected because their evolutionary consequences are complex, unpredictable, or seen as transient, we argue that they warrant further attention in a rapidly warming world.

Citation

Chirgwin E, Marshall DJ, Sgrò CM, Monro K (2016) The other 96%: Can neglected sources of fitness variation offer new insights into adaptation to global change? Evolutionary Applications, PDF DOI

Incorporating evolutionary adaptation in species distribution modelling reduces projected vulnerability to climate change

Authors: Alex Bush, Karel Mokany, Renee Catullo, Ary Hoffmann, Vanessa Kellermann, Carla Sgrò, Shane McEvey, and Simon Ferrier

Published in: Ecology Letters, volume 19, issue 12 (December 2016)

Abstract

Based on the sensitivity of species to ongoing climate change, and numerous challenges they face tracking suitable conditions, there is growing interest in species’ capacity to adapt to climatic stress.

Here, we develop and apply a new generic modelling approach (AdaptR) that incorporates adaptive capacity through physiological limits, phenotypic plasticity, evolutionary adaptation and dispersal into a species distribution modelling framework.

Using AdaptR to predict change in the distribution of 17 species of Australian fruit flies (Drosophilidae), we show that accounting for adaptive capacity reduces projected range losses by up to 33% by 2105. We identify where local adaptation is likely to occur and apply sensitivity analyses to identify the critical factors of interest when parameters are uncertain.

Our study suggests some species could be less vulnerable than previously thought, and indicates that spatiotemporal adaptive models could help improve management interventions that support increased species’ resilience to climate change.

Citation

Bush A, Mokany K, Catullo R, Hoffmann A, Kellermann V, Sgrò C, McEvey S, Ferrier S (2016) Incorporating evolutionary adaptation in species distribution modelling reduces projected vulnerability to climate change. Ecology Letters, PDF DOI