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

Limited scope for plasticity to increase upper thermal limits

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

Published in: Functional Ecology, volume 30, issue 12 (December 2016)

Summary

Increases in average temperature and the frequency of extreme temperature events are likely to pose a major risk to species already close to their upper physiological thermal limits. The extent to which thermal phenotypic plasticity can buffer these changes and whether plasticity is constrained by basal tolerance levels remains unknown.

We examined the effect of developmental temperature under both constant and fluctuating thermal regimes (developmental acclimation), as well as short-term heat hardening, on upper thermal limits (CTmax) in a tropical and temperate population of Drosophila melanogaster.

We found evidence for thermal plasticity in response to both developmental acclimation and hardening treatments; CTmax increased at warmer developmental temperatures and with a prior heat hardening treatment. However, hardening and acclimation responses were small, improving CTmax by a maximum of 1·01 °C. These results imply that overheating risk will only be minimally reduced by plasticity.

We observed significant associations between developmental temperature and both basal CTmax and hardening capacity (a measure of the extent of the plastic response). Basal CTmax increased, while hardening capacity decreased, with increasing developmental acclimation temperature. This indicates that increases in basal heat resistance at warmer temperatures may come at the cost of a reduced capacity to harden.

While plasticity in CTmax is evident in both populations of D. melanogaster we studied, plastic increases in upper thermal limits, particularly at warmer temperatures, may not be sufficient to keep pace with temperature increases predicted under climate change.

Citation

van Heerwaarden B, Kellerman V, Sgrò CM (2016) Limited scope for plasticity to increase upper thermal limits. Functional Ecology PDF DOI

Thermal plasticity in Drosophila melanogaster populations from eastern Australia: quantitative traits to transcripts

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

Published in: Journal of Evolutionary Biology, volume 29, issue 12 (December 2016)

Abstract

The flexibility afforded to genotypes in different environments by phenotypic plasticity is of interest to biologists studying thermal adaptation because of the thermal lability of many traits. Differences in thermal performance and reaction norms can provide insight into the evolution of thermal adaptation to explore broader questions such as species distributions and persistence under climate change.

One approach is to study the effects of temperature on fitness, morphological and more recently gene expression traits in populations from different climatic origins. The diverse climatic conditions experienced by Drosophila melanogaster along the eastern Australian temperate-tropical gradient are ideal given the high degree of continuous trait differentiation, but reaction norm variation has not been well studied in this system.

Here, we reared a tropical and temperate population from the ends of the gradient over six developmental temperatures and examined reaction norm variation for five quantitative traits including thermal performance for fecundity, and reaction norms for thermotolerance, body size, viability and 23 transcript-level traits.

Despite genetic variation for some quantitative traits, we found no differentiation between the populations for fecundity thermal optima and breadth, and the reaction norms for the other traits were largely parallel, supporting previous work suggesting that thermal evolution occurs by changes in trait means rather than by reaction norm shifts.

We examined reaction norm variation in our expanded thermal regime for a gene set shown to previously exhibit G×E for expression plasticity in east Australian flies, as well as key heat-shock genes.

Although there were differences in curvature between the populations suggesting a higher degree of thermal plasticity in expression patterns than for the quantitative traits, we found little evidence to support a role for genetic variation in maintaining expression plasticity.

Citation

Clemson AS, Sgrò CM, Telonis-Scott M (2016) Thermal plasticity in Drosophila melanogaster populations from eastern Australia: quantitative traits to transcripts. Journal of Evolutionary Biology PDF DOI

The effect of temperature on Wolbachia-mediated dengue virus blocking in Aedes aegypti

Authors: Yixin H Ye, Alison M Carrasco, Yi Dong, Carla M Sgrò and Elizabeth A McGraw

Published in: The American Society of Tropical Medicine and Hygiene, volume 94 issue 4 (April 2016)

Abstract

Dengue fever, caused by dengue virus (DENV), is endemic in more than 100 countries. The lack of effective treatment of patients and the suboptimal efficacies of the tetravalent vaccine in trials highlight the urgent need to develop alternative strategies to lessen the burden of dengue fever.

Wolbachia pipientis, an obligate intracellular bacterium, is being developed as a biocontrol strategy against dengue because it limits the replication of the DENV in the mosquito vector, Aedes aegypti. However, several recent studies have demonstrated the sensitivity of pathogens, vectors, and their symbionts to temperature.

To understand how the tripartite interactions between the mosquito, DENV, and Wolbachia may change under different temperature regimes, we assessed the vector competence and transmission potential of DENV-infected mosquitoes reared at a common laboratory setting of a constant 25°C and at two diurnal temperature settings with mean of 25°C and 28°C and a fluctuating range of 8°C (±4°C).

Temperature significantly affected DENV infection rate in the mosquitoes. Furthermore, temperature significantly influenced the proportion of mosquitoes that achieved transmission potential as measured by the presence of virus in the saliva. Regardless of the temperature regimes, Wolbachia significantly and efficiently reduced the proportion of mosquitoes achieving infection and transmission potential across all the temperature regimes studied.

This work reinforces the robustness of the Wolbachia biocontrol strategy to field conditions in Cairns, Australia, and suggests that similar studies are required for local mosquito genotypes and field relevant temperatures for emerging field release sites globally.

Citation

Ye YH, Carrasco AM, Dong Y, Sgrò CM, McGraw EM (2016) The effect of temperature on Wolbachia-mediated dengue virus blocking in Aedes aegypti. American Journal of Tropical Medicine and Hygiene PDF DOI

Drosophila as models to understand the adaptive process during invasion

Authors: Patricia Gibert , Matthew Hill, Marta Pascual, Christophe Plantamp, John S Terblanche, Amir Yassin and Carla M Sgrò

Published in: Biological Invasions, volume 18, issue 4 (April 2016)

Abstract

The last few decades have seen a growing number of species invasions globally, including many insect species.

In drosophilids, there are several examples of successful invasions, i.e. Zaprionus indianus and Drosophila subobscura some decades ago, but the most recent and prominent example is the invasion of Europe and North America by the pest species, Drosophila suzukii.

During the invasive process, species often encounter diverse environmental conditions that they must respond to, either through rapid genetic adaptive shifts or phenotypic plasticity, or by some combination of both. Consequently, invasive species constitute powerful models for investigating various questions related to the adaptive processes that underpin successful invasions.

In this paper, we highlight how Drosophila have been and remain a valuable model group for understanding these underlying adaptive processes, and how they enable insight into key questions in invasion biology, including how quickly adaptive responses can occur when species are faced with new environmental conditions.

Citation

Gibert P, Hill M, Pascual M, Plantamp C, Terblanche JS, Yassin A, Sgrò, CM (2016) Drosophila as models to understand the adaptive process during invasion. Biological Invasions PDF DOI

PhD project: The role of nutrition in mediating evolutionary responses to rapid environmental change

Update: this position is now filled.

A fully-funded PhD stipend is available for a suitably qualified student interested in working on the evolutionary responses to environmental change, with particular reference to the genetic and physiological pathways that mediate the role of nutrition in adaptation to change.

The project will be supervised by Associate Professor Carla Sgrò, School of Biological Sciences, Monash University, Melbourne, Australia.

Studies attempting to understand organismal responses to climate change have focussed on climatic stressors. However food limitation is one of the most common environmental challenges faced by organisms. How energy intake is balanced to optimise fitness under changing climates, and how this affects the capacity of organisms to respond to climate change, is unknown.

This project will combine genomics, developmental genetics and experimental evolution, within the geometric framework for nutrition, to understand how nutrition mediates evolutionary responses to environmental change. It will do so by identifying the genetic and physiological pathways that mediate the role of nutrition in adaptation to environmental change.

Successful candidates will be fully funded for 3.5 years (the length of a PhD in Australia), for full-time research, and with no teaching requirements. The annual stipend is approximately $25,000 AUD tax-free (equivalent to approximately $33,000 before tax) with additional expenses for research, coursework, and conference attendance (once per year) also covered.

To apply, please send a CV and academic transcript to carla.sgro@monash.edu.

Applicants must hold a Bachelor’s degree with first-class honours, or a master’s degree.

Review of applications will begin immediately, and short-listed candidates will be contacted to set up interviews via phone or Skype.